Primary Auditory Fields Research Articles

Representation of frequency in the primary auditory field of the barn owl forebrain.

1. The primary auditory field (PAF) constitutes the first telencephalic stage of auditory information processing in the classical auditory pathway. In this study we investigated the frequency representation in the PAF of the barn owl, a species with a broad frequency range of hearing and a highly advanced auditory system. 2. Single- and multiunit sites were recorded extracellularly in ketamine-anesthetized owls. The frequency response properties of PAF sites were assessed with the use of digitally synthesized dichotic stimuli. PAF sites (n = 442) either were unresponsive to tonal stimulation (but responsive to noise stimuli), were tuned for frequency, or had multipeaked frequency response profiles. Tuned sites responded best to frequencies between 0.2 and 8.8 kHz, a range that encompasses nearly the entire hearing range of the barn owl. Most sites responding best to frequencies < 4 kHz had relatively broad frequency tuning, whereas sites responding best to higher frequencies had either broad or narrow frequency tuning. Sites with multipeaked frequency response profiles typically had two response peaks. The first peak was usually between 1 and 3 kHz and the second was usually between 5 and 8 kHz; there was no systematic relationship between the two peak frequencies. 3. In dorsoventral electrode penetrations that contained sites with tuned and/or multipeaked response profiles, a "common frequency" was identified that elicited a maximal response from all of the sites in the penetration. 4. The PAF contains a single tonotopic field. Units tuned to low frequencies are located caudomedially, whereas units tuned to high frequencies are located rostrolaterally. Compared with the frequency representation along the basilar papilla and in other auditory structures, the PAF overrepresents low frequencies (< 4 kHz) that are important for barn owl vocalizations. Conversely, high frequencies (> or = 4 kHz), which are necessary for precise sound localization, are underrepresented relative to these more peripheral auditory structures. 5. There was considerable interindividual variability both in the relative magnification of different frequency ranges and in the orientation of the tonotopic map in the brain. 6. These results suggest that the barn owl PAF, like the mammalian primary auditory cortex, is a general processor of auditory information that is involved in the analysis of both the meaning (such as species-specific vocalizations) and the location of auditory stimuli. In addition, the high degree of interindividual variability in the representation of frequency information suggests that the barn owl PAF, like the mammalian auditory cortex, is subject to modification by sensory experience.

Response properties of units in the posterior auditory field deprived of input from the ipsilateral primary auditory cortex

The influence of the ipsilateral primary auditory field (Al) on the response properties of neurons in the posterior auditory field (Field P) was examined in three cats anesthetized with sodium pentobarbital. Rate/level functions were obtained, by extracellular recording, from single units in Field P before ( n = 38) and after ( n = 50) subpial aspiration of AI. The ablations were primarily confined to the medial ectosylvian gyrus, although in one case extended into the high-frequency portion of the anterior auditory field. Comparisons between the behavior of units isolated before and after Al ablation failed to demonstrate any changes in the response properties of neurons in Field P attributable to the ablation. Nonmonotonic response profiles, first spike latency, variability in latency, threshold and maximal discharge rates of the units to acoustic stimuli were not significantly altered by the AI ablation. These results indicate that the basic response properties of neurons in Field P do not depend on input from the ipsilateral AI. This suggests that these properties are most likely determined by thalamic input or by circuitry within Field P.

Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds.

The neural response to amplitude-modulated sinus sounds (AM sound) was investigated in the auditory cortex and insula of the awake squirrel monkey. It was found that 78.1% of all acoustically driven neurons encoded the envelope of the AM sound; the remaining 21.9% displayed simple On, On/Off or Off responses at the beginning or the end of the stimulus sound. Those neurons with AM coding were able to encode the AM sound frequency in two different ways: (1) the spikes followed the amplitude modulation envelopes in a phase locked manner; (2) the spike rate changed significantly with changing modulation frequencies. As reported in other species, the modulation transfer functions for rate showed higher modulation frequencies than the phase-locked response. Both AM codings exhibited a filter characteristic for AM sound. Whereas 46.6% of all neurons had the same filter characteristic for both the spike discharge and the phase-locked response, the remaining neurons displayed combinations of different filter types. The discharge pattern of a neuron to simple tone or noise bursts suggests the behaviour of this neuron when AM sound is used as the stimulus. Neurons with strong onset responses to tone/noise bursts tended to have higher phase-locked AM responses than neurons with weak onset responses. The spike rate maxima for AM sound showed no relation to the tone/noise burst discharge patterns. Varying modulation depth was encoded by the neuron's ability to follow the envelope cycles and not by the non-phase-locked spike rate frequency. The organization of the squirrel monkey's auditory cortex has previously been established by an anatomical study. We have added two new fields using physiological parameters. All fields investigated showed a clear functional separation for time-critical information processing. The best temporal resolution was shown by the primary auditory field (AI), the first-temporal field (T1) and the parainsular auditory field (Pi). The neural data in these fields and the amplitude modulation frequency range of squirrel monkey calls suggest a similar correlation between vocalization and perception as in human psychophysical data for speech and hearing sensation. The anterior fields in particular failed to follow the AM envelopes. For the first time in a primate, the insula was tested with different sound parameters ranging from simple tone bursts to AM sound. It is suggested that this cortical region plays a role in time-critical aspects of acoustic information processing. The observed best frequencies covered the same spectrum as AI. As in the auditory fields, most neurons in the insula encoded AM sound with different filter types. The high proportion of neurons unable to encode AM sound (40.6%) and the low mean best modulation frequency (9.9 Hz) do not support a prominent role of the insula in temporal information processing.

Comparison of Frequency‐specific c‐Fos Expression and Fluoro‐2‐deoxyglucose Uptake in Auditory Cortex of Gerbils (Meriones unguiculatus)

Induction of c-Fos in the auditory cortex of gerbils was investigated immunocytochemically 1 h after single, triple or 1 h continuous stimulation with a series of narrow band frequency-modulated tone bursts. With single stimulation c-Fos immunoreactive neurons were chiefly found in the primary auditory field (AI), where they formed a narrow frequency-specific column across layers II-VI. Side-band-like patterns adjacent to this column appeared characteristically with triple stimulation. Immunoreactive cell density in the anterior auditory field and the caudal fields was sparse and location not frequency specific with single or triple stimulation. Spatial comparisons of c-Fos immunoreactive neuron density with 2-deoxy-2-fluoro-D-glucose (FDG) autoradiography in the same animals after 1 h of stimulation revealed spreading of c-Fos expression in neurons across the tonotopic maps of the AI and in the rostral and caudal fields of the auditory cortex. The pattern of the highest density of c-Fos labelled cells in the AI still matched the peak labelling of FDG autoradiographs. The results show that the postsynaptic marker c-Fos reflects the frequency representation in the AI with single or triple stimulation yet with a higher spatial resolution than the deoxyglucose technique. Longer stimulation causes nontonotopic intracortical spreading of the c-Fos-inducing message, a phenomenon potentially reflecting the effects of cooperativity in the maps.

The auditory pathway in cat corpus callosum.

The cortical auditory fields of the two hemispheres are interconnected via the corpus callosum. We have investigated the topographical arrangement of auditory callosal axons in the cat. Following circumscribed biocytin injections in the primary (AI), secondary (AII), anterior (AAF) and posterior (PAF) auditory fields, labelled axons have been found in the posterior two-thirds of the corpus callosum. Callosal axons labelled by small individual cortical injections did not form a tight bundle at the callosal midsagittal plane but spread over as much as one-third of the corpus callosum. Axons originating from different auditory fields were roughly topographically ordered, reflecting to some extent the rostro-caudal position of the field of origin. Axons from AAF crossed on average more rostrally than axons from AI; the latter crossed more rostrally than axons from PAF and AII. Callosal axons originating in a discrete part of the cortex travelled first in a relatively tight bundle to the telo-diencephalic junction and then dispersed progressively. In conclusion, the cat corpus callosum does not contain a sector reserved for auditory axons, nor a strictly topographically ordered auditory pathway. This observation is of relevance to neuropsychological and neuropathological observations in man.

Comparison of responses in the anterior and primary auditory fields of the ferret cortex

1. Characteristics of an anterior auditory field (AAF) in the ferret auditory cortex are described in terms of its electrophysiological responses to tonal stimuli and compared with those of primary auditory cortex (AI). Ferrets were barbiturate-anesthetized and tungsten microelectrodes were used to record single-unit responses from both AI and AAF fields. Units in both areas were presented with the same stimulus paradigms and their responses analyzed in the same manner so that a direct comparison of responses was possible. 2. The AAF is located dorsal and rostral to AI on the ectosylvian gyrus and extends into the suprasylvian sulcus rostral to AI. The tonotopicity is organized with high frequencies at the top of the sulcus bordering the high-frequency area of AI, then reversing with lower BFs extending down into the sulcus. AAF contained single units that responded to a frequency range of 0.3-30 kHz. 3. Stimuli consisted of single-tone bursts, two-tone bursts and frequency-modulated (FM) stimuli swept in both directions at various rates. Best frequency (BF) range, rate-level functions at BF, FM directional sensitivity, and variation in asymmetries of response areas were all comparable characteristics between AAF and AI. Responses in both areas were primarily phasic. 4. The characteristics that were different between the two cortical areas were: latency to tone onset, excitatory bandwidth 20 dB above threshold (BW20), and preferred FM rate as parameterized with the centroid (a weighted average of spike counts). The mean latency of AAF units was shorter than in AI (AAF: 16.8 ms, AI: 19.4 ms). BW20 measurements in AAF were typically twice as large as those found in AI (AAF: 2.5 octaves, AI 1.3 octaves). The AI centroid population had a significantly larger standard deviation than the AAF centroid population. 5. We examined the relationship between centroid and BW20 to see whether wider bandwidths were a factor in a unit's ability to detect fast sweeps. There was significant (P < 0.05) linear correlation in AAF but not in AI. In both fields the variance of the centroid population decreased with increasing BW20. BW20 decreased as BF increased for units in both auditory fields.

Auditory cortex of the rufous horseshoe bat: 1. Physiological response properties to acoustic stimuli and vocalizations and the topographical distribution of neurons.

The extent and functional subdivisions of the auditory cortex in the echolocating horseshoe bat, Rhinolophus rouxi, were neurophysiologically investigated and compared to neuroarchitectural boundaries and projection fields from connectional investigations. The primary auditory field shows clear tonotopic organization with best frequencies increasing in the caudorostral direction. The frequencies near the bat's resting frequency are largely over-represented, occupying six to 12 times more neural space per kHz than in the lower frequency range. Adjacent to the rostral high-frequency portion of the primary cortical field, a second tonotopically organized field extends dorsally with decreasing best frequencies. Because of the reversed tonotopic gradient and the consistent responses of the neurons, the field is comparable to the anterior auditory field in other mammals. A third tonotopic trend for medium and low best frequencies is found dorsal to the caudal primary field. This area is considered to correspond to the dorsoposterior field in other mammals. Cortical neurons had different response properties and often preferences for distinct stimulus types. Narrowly tuned neurons (Q10dB > 20) were found in the rostral portion of the primary field, the anterior auditory field and in the posterior dorsal field. Neurons with double-peaked tuning curves were absent in the primary area, but occurred throughout the dorsal fields. Vocalization elicited most effectively neurons in the anterior auditory field. Exclusive response to pure tones was found in neurons of the rostral dorsal field. Neurons preferring sinusoidal frequency modulations were located in the primary field and the anterior and posterior dorsal fields adjacent to the primary area. Linear frequency modulations optimally activated only neurons of the dorsal part of the dorsal field. Noise-selective neurons were found in the dorsal fields bordering the primary area and the extreme caudal edge of the primary field. The data provide a survey of the functional organization of the horseshoe bat's auditory cortex in real coordinates with the support of cytoarchitectural boundaries and connectional data.

Interhemispheric connections in neonatal owl monkeys ( Aotus trivirgatus) and galagos ( Galago crassicaudatus)

Interhemispheric connections were studied by injecting a mixture of horseradish peroxidase (HRP) and wheatgerm agglutinin conjugated with horseradish peroxidase (WGA-HRP) into multiple sites in dorsolateral occipital and parietal cortex of one cerebral hemisphere of three galagos ( Galago crassicaudatus) and two owl monkeys ( Aotus trivirgatus) within seven days of birth. Cortex was either separated from the rest of the brain, flattened and cut parallel to the surface to aid reconstructing surface-view patterns of labeled neurons and processes, or cut in standard coronal or parasagittal planes to better reveal laminar patterns of connections. In both primate species, the surface-view pattern of callosal connections in infants was remarkably adult-like. In infant owl monkeys, callosal connections were concentrated along the margin of area 18 with area 17, and only a few labeled cells were found within area 17. Other visual areas including the second visual area, V-II, and the middle temporal visual area, MT, had patchy distributions of labeled neurons that extended over large parts of the visual field representations. Primary motor, auditory, and somatosensory fields also had patchy distributions of labeled neurons, with regions of areas 3b and adjoining somatosensory fields having few callosal connections in portions that appeared to correspond with representations of the hand and foot. Results were very similar in galagos, except that newborn galagos, as in adults, had a patchy distribution of callosally projecting neurons that extended well within area 17. Furthermore, the labeled neurons were concentrated in patches that aligned with the cytochrome oxidase blobs of area 17. Finally, callosal connections were concentrated in cytochrome oxidase poor regions of area 3b.

Several neuronal and axonal types form long intrinsic connections in the cat primary auditory cortical field (AI).

Intrinsic connections in the cat primary auditory field (AI) as revealed by injections of Phaseolus vulgaris leucoagglutinin (PHA-L) or biocytin, had an anisotropic and patchy distribution. Neurons, labelled retrogradely with PHA-L were concentrated along a dorsoventral stripe through the injection site and rostral to it; the spread of rostrally located neurons was greater after injections into regions of low rather than high characteristic frequencies. The intensity of retrograde labelling varied from weak and granular to very strong and Golgi-like. Out of 313 Golgi like retrogradely labelled neurons 79.6% were pyramidal, 17.2% multipolar, 2.6% bipolar, and 0.6% bitufted; 13.4% were putatively inhibitory, i.e. aspiny or sparsely spiny multipolar, or bitufted. Individual anterogradely labelled intrinsic axons were reconstructed for distances of 2 to 7 mm. Five main types were distinguished on the basis of the branching pattern and the location of synaptic specialisations. Type 1 axons travelled horizontally within layers II to VI and sent collaterals at regular intervals; boutons were only present in the terminal arborizations of these collaterals. Type 2 axons also travelled horizontally within layers II to VI and had rather short and thin collateral branches; boutons or spine-like protrusions occurred in most parts of the axon. Type 3 axons travelled obliquely through the cortex and formed a single terminal arborization, the only site where boutons were found. Type 4 axons travelled for some distance in layer I; they formed a heterogeneous group as to their collaterals and synaptic specializations. Type 5 axons travelled at the interface between layer VI and the white matter; boutons en passant, spine-like protrusions, and thin short branches with boutons en passant were frequent all along their trajectory. Thus, only some axonal types sustain the patchy pattern of intrinsic connectivity, whereas others are involved in a more diffuse connectivity.

Functional Organization of Auditory Cortex in the Mongolian Gerbil (Meriones unguiculatus). I. Electrophysiological Mapping of Frequency Representation and Distinction of Fields

The frequency representation within the auditory cortex of the anaesthetized Mongolian gerbil (Meriones unguiculatus) was studied using standard microelectrode (essentially multiunit) mapping techniques. A large tonotopically organized primary auditory field (AI) was identified. High best frequencies (BFs) were represented rostrally and low BFs caudally along roughly dorsoventrally oriented isofrequency contours. Additional tonotopic representations were found adjacent to AI. Rostral to AI was a smaller field with a complete tonotopic gradient reversed with respect to that in AI (mirror image representation) and was termed the anterior auditory field (AAF). BFs in the range from 0.1 to 43 kHz, apparently covering the hearing range of the Mongolian gerbil, were found in AI and AAF. Units in these two core fields responded to narrow frequency ranges with short latencies. Ventral to the common high-frequency border to AAF and AI, a rapid transition to very low BFs suggested the presence of a ventral field (V). Caudal to AI two small tonotopically organized fields were identified, a dorsoposterior field (DP) and a ventroposterior field (VP). The VP showed a tonotopic organization mirror imaged to that of AI, i.e. low frequencies were represented rostrally near the caudal border of AI, and high frequencies caudally. The DP showed a concentric frequency organization with high BFs located in the centre. Units in DP and VP fired less strongly, with considerably longer latencies, and responded to a broader range of frequencies than units in AI and AAF. Dorsocaudal to AI a dorsal field (D) was identified, harbouring units that responded to very broad ranges of frequencies. A tonotopic organization of field D could not be discerned. In the border region of AI and D, low-frequency responses were similar to those found in parts of AI and AAF, but without a clear-cut tonotopic organization. This region was termed Ald. The two core fields AI and AAF appeared to be located within the koniocortex, while the remaining fields lay outside. Our data show that the organization of the gerbil auditory cortex is highly elaborate, with parcellation into fields as complex as in cat or primates.

Functional organization of auditory cortex in the mongolian gerbil (Meriones unguiculatus). II. Tonotopic 2-deoxyglucose.

The tonotopic organization of the auditory cortex in the Mongolian gerbil was mapped with 2-deoxyfluoro-D-glucose (2DG) using narrow-band frequency-modulated tones of different centre frequency (FM tones) and tones periodically alternating between two different frequencies (alternating tones) as stimuli. Continuous tone bursts of a constant frequency and repetition rate were used in initial experiments. Continuous tones produced 2DG patterns similar to those observed in animals that were not specifically stimulated. With tone bursts of constant frequency and repetition rate variable patterns were observed, some of which could be interpreted only in retrospect in the light of results obtained with FM tones and alternating tones. These stimuli, in contrast, produced differential metabolic responses which in conjunction with 2DG data from monaural animals and electrophysiological data made it possible to distinguish a primary auditory field AI with its dorsal region Ald, an anterior auditory field AAF, a ventral field V, a dorsoposterior field DP and a ventroposterior field VP, a dorsal field D, and in addition an anteroventral field AV. In the largest field (AI) and the smaller rostrally adjacent field AAF, frequency-specific dorsoventral bands of labelling (isofrequency contours) were mapped quantitatively. Bands shifted as a function of frequency relative to each other and to an independent spatial reference line in the lateral hippocampus. Spatial analysis of the single bands obtained with FM tones, and of the double bands obtained with alternating tones in both fields, revealed roughly mirror-imaged tonotopic maps of AI and AAF. In AI the progression from low to high frequencies was from caudal to rostral and in AAF the gradient was reversed, leading to a common high-frequency border of the two fields. In AI, the spatial resolution for frequencies below 16 kHz was in similar intervals per octave and higher for frequencies below 1 kHz. AI showed a somewhat higher spatial resolution for frequencies (at least below 1 kHz) as well as longer isofrequency contours than AAF. The 2-deoxyglucose patterns provided average tonotopic maps and topological data on various fields, as well as reliable landmarks in the gerbil's auditory cortex.

Subdivisions and connections of auditory cortex in owl monkeys

The organization and connections of auditory cortex in owl monkeys, Aotus trivirgatus, were investigated by combining microelectrode mapping methods with studies of architecture and connections in the same animals. In most experiments, portions of auditory cortex were first explored with microelectrodes, neurons were characterized as responsive or not to auditory stimuli, and best frequencies were determined whenever possible. Most recordings were in cortex previously designated as primary (A-I) and rostral (R) auditory fields (Imig et al. J Comp Neurol 171:111, '77) and in a newly defined rostrotemporal field (RT) located rostral to R. Injections of wheat germ agglutinin-horseradish peroxidase (WGA-HRP) and fluorescent tracers were placed in electrophysiologically identified locations of A-I, R, and RT; the posterolateral (PL) and anterolateral (AL) divisions of a narrow belt of auditory cortex lateral and adjacent to A-I and R; cortex of the superior temporal gyrus lateral and rostrolateral to PL and AL; and regions of prefrontal cortex that receive inputs from auditory cortex. There were several major findings: 1. Best frequencies were most clearly determined for neurons within a densely myelinated strip of cortex on the lower bank and lip of the lateral sulcus. We divided this strip into three fields, A-I, R, and RT, although an alternative interpretation that A-I and R are parts of a single field remains tenable. In some cases, isofrequency contours appeared to continue uninterrupted across fields A-I and R, with lower frequencies represented laterally and higher frequencies represented deeper in the sulcus. In other cases, there was a tendency for high frequencies to be represented caudally and medially, and low frequencies laterally in A-I and rostrally in R, with partial discontinuity in the isofrequency contours. A reversal of the tonotopic gradient appeared in RT with a common low-frequency representation at the caudal border with R, and progressively higher frequencies encountered rostrally. Of the three fields, A-I appears slightly more myelinated than R, and RT slightly less than R. The distinctiveness of the three fields is further demonstrated by the patterns of connections. In particular, A-I and RT are both interconnected with R, but not with each other. Connections between A-I and R are between tonotopically matched locations. 2. A narrow 2-3 mm wide band of cortex lateral to A-I, R, and RT was also responsive to auditory stimuli, but typically neurons were more difficult to activate, and best frequencies were more difficult to determine. No distinctions in myeloarchitecture or CO activity were obvious.(ABSTRACT TRUNCATED AT 400 WORDS)

Functional Topographies in the Primary Auditory Cortex of the Cat

One of the fundamental organizational principles of the mammalian sensory cortex is the topographic representation of the sensory epithelium. A cochleotopic topographic organization has been demonstrated for a number of auditory cortical fields, including the primary auditory field (AI). In the spatial cortical dimension orthogonal to the cochleotopic frequency gradient, systematic arrangements of other functional parameters have been observed. The first evidence of a spatial segregation of functional parameters along the isofrequency domain of cat AI was the discovery of binaural interaction bands. Recent studies show topographic representations of additional functional parameters in the central auditory system of the cat. Among the functional parameters that are evidence of systematic and topographic representations in cat auditory cortical fields are spectral resolution (sharpness of tuning), temporal resolution (preferred repetition rate), and inhibitory properties related to the coding of broadband signals.

Correlation between regional changes in the distributions of GABA-containing neurons and unit response properties in the medial geniculate body of the cat

A consistent change in the distribution of single units as a function of several of their properties of response to clicks, noise and tone bursts was observed along the rostro-caudal axis in the ventral division of the medial geniculate body (vMGB). From posterior to anterior, the proportion of inhibitory response patterns and non-monotonic intensity functions progressively decreased; response latencies were progressively shorter and less dispersed from caudal to rostral. This functional heterogeneity is consistent with the segregation of the thalamocortical interconnections: the anterior part of vMGB projects to the anterior and primary auditory cortical fields, whereas the posterior part of vMGB projects mainly to the posterior auditory cortical field. Changes in the distribution of response properties from posterior to anterior in vMGB were found to be correlated with a progressive decrease of the density of GABA-immunoreactive neurons from caudal to rostral. Since GABAergic neurons in sensory thalamic nuclei are believed to be interneurons, these data suggest that interneurons might contribute to regional changes in the distribution of some response properties along the rostro-caudal axis in vMGB. In particular, the high proportion of inhibitory response patterns and non-monotonic intensity functions in the posterior vMGB might well be related to the high density of GABA-containing neurons caudally, where they exert a strong inhibitory influence on principal cells. Intrinsic neurons might contribute to the segregation of the acoustic information transferred from vMGB to the various auditory cortical fields. In contrast, no clear and systematic change in the distribution of response properties along the rostro-caudal axis was observed in the medial division of the MGB, in which the GABA-immunoreactive neurons were evenly distributed.

Anatomical study of the connections of the primary auditory area in the rat.

The aim of the present study was to identify in the rat the overall input-output pattern of connections of the primary auditory field, with special attention to the topographical organization of the geniculocortical auditory projection. By using cytoarchitectural criteria, three temporal cortical fields were distinguished in the rat: Te1, Te2, and Te3. The primary auditory field Te1 is characterized by a relatively specific differentiation of its layers when compared with other temporal fields. The afferent and efferent connections of Te1 were identified by using the retrograde and anterograde transport of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP). The results indicate that Te1 is connected by a dense and reciprocal system of fibers with the auditory thalamus. Based on the nomenclature of Morest ('64) in the cat, five cytoarchitectural subdivisions of the medial geniculate complex (MG) were identified in the rat: ventral (MGv), dorsal (MGd), medial (MGm), suprageniculate (Sg), and peripeduncular (PPA). The major rostrocaudal extent of the MGv is connected to Te1. The surrounding cortical fields Te2 and Te3 do not receive a projection from the MGv, except from its most caudal pole. The MGv projection is topographically organized. When the deposit area of the tracer is shifted from dorsal to ventral upon Te1, the corresponding labeled zone within the MGv moves from rostral to caudal, whereas a cortical displacement of the deposit area of the tracer from rostrodorsal to caudoventral leads to a medial to lateral shift of the labeled zone in the MGv. In addition, more dorsal parts of the MGv project on more dorsal sectors of Te1. Te1 receives a sparser, topographically organized projection from the deep dorsal subdivision of the MGd. The MGm and the lateral part of the posterior group of thalamic nuclei (Pol) also distribute fibers to the primary auditory field. Te1 is reciprocally connected by a system of callosal fibers with the contralateral homotypic cortex. Finally, Te1 sends fibers to the dorsal and, to a lesser extent, external cortices of the inferior colliculus, caudomedial caudate-putamen complex, and caudoventral thalamic reticular nucleus.

Functional organization of the medial division of the medial geniculate body of the cat: Tonotopic organization, spatial distribution of response properties and cortical connections

The discharge properties of 735 single units located in the pars magnocellularis (M) of the medial division of the medial geniculate body (MGB) were studied in 23 nitrous oxide anesthetized cats in response to simple acoustic stimuli (clicks, noise and tone bursts). A systematic decrease of single unit characteristic frequencies (CF) was observed along electrode track portions crossing M from dorso-medial to ventro-lateral. These data indicate that M is tonotopically organized with an arrangement of low CF units latero-ventrally and high CF units dorso-medially. This preferential arrangement of single units as a function of their CF was consistent with the location and orientation of clusters of labeled cells in M resulting from wheat-germ agglutinin labeled with horseradish peroxidase (WGA-HRP) injections in CF defined loci in the anterior (AAF) or primary (AI) auditory cortical fields. The quality of the tonotopic arrangement was low caudally and increased in the rostral direction, indicating that this tonotopicity concerns mainly the anterior half of M. Response latencies to clicks, noise and tone bursts were on average longer in the posterior part of M than in its anterior part. Time-locking of discharges in response to repetitive acoustic pulses was more frequent anteriorly than posteriorly and the upper limiting rate of locking was on average higher rostrally (up to 200–300 Hz). In contrast, other response properties such as responsiveness to the various combinations of simple acoustic stimuli, response patterns and tuning were more randomly distributed in M, showing the whole range of respoase properties seen in the MGB. Data derived from several injections of WGA-HRP performed in distinct auditory cortical fields in several animals indicated that M projects to the tonotopic cortical fields (AAF, AI and PAF) as well as to the non-tonotopically organized secondary auditory cortex (AII). The contribution of M to the total thalamic input reaching each field of the auditory cortex was quantitatively more important for AAF (30%) and PAF (20%) than for AI and AII (about 10% each).

Sensitivity of Single Neurons in Auditory Cortex to Contour: Toward a Neurophysiology of Music Perception

The responses of single neurons in the primary (AI) and secondary (AII) auditory cortical fields of waking cats were recorded during presentation of sequences of five iso-intensity tones. Tonal contour was varied by employing sequences that either increased or decreased monotonically in frequency, or in which contour was non-monotonic. The vast majority of neurons in both auditory fields (84%) exhibited sensitivity to tonal contour, that is, the response to at least one frequency (usually more) in a sequence differed significantly between two or more types of contour. Although all of the mechanisms involved have not been identified, the serial position of a tone within a sequence could explain some of the findings. Responsivity may also depend upon the magnitude of the interval difference between two consecutive tones. Additionally, contour per se could be effective even for neurons that were not sensitive to differences in type of contour; for example, responses to the same tones could be facilitated when presented in sequences of different frequencies compared to sequences of the same frequency. Further, the range of frequency response and the best frequency of a neuron may depend upon whether these parameters are determined using isolated tones or contoured sequences. Finally, omission of one tone within a sequence produced significant modification of response to other tones in most (87%) cells, with effects extending up to 3 sec following the the gap. Neurons in both primary and secondary auditory cortical fields displayed all effects, the only difference was that neurons in All were more likely to exhibit sensitivity to tone omission than those in AI. The findings are discussed with reference to neurophysiological and psychophysical data. We conclude that the effects of contour and other aspects of tonal sequences are detectable at the level of single neurons in auditory cortex of waking animals and that the use of dynamic stimuli is likely to be critical for a neurophysiological account of music perception and the perception of other complex acoustic stimuli.

Cortical connections of electrophysiologically and architectonically defined subdivisions of auditory cortex in squirrels.

Multiunit recordings with microelectrodes were used to identify and delimit subdivision of auditory cortex in squirrels. In the same animals, cortical connections of subdivisions of auditory cortex were determined by placing injections of the tracer wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) into electrophysiologically defined locations. The electrophysiological results and patterns of connections were later related to myeloarchitectonic distinctions in brain sections cut parallel to the surface of the artificially flattened cortex. As previously described (Merzenich et al.: J. Comp. Neurol. 166:387-402, '76), a primary auditory field, A-I, was characterized by (1) neurons narrowly tuned to tone frequency; (2) a tonotopic map with high frequencies, which represented caudal to low frequencies; and (3) dense myelination. A-I was reciprocally connected with a rostral field, R, a parietal ventral somatosensory representation, PV, cortex ventral to A-I, and other nearby regions of cortex of the same hemisphere. Callosal connections of A-I were with A-I, R, and two or more other regions of temporal cortex. The less densely myelinated rostral field, R, also had neurons that were frequency tuned, but the neurons were often less securely driven. R appeared to have a tonotopic organization that roughly mirrored that of A-I. Ipsilateral connections of R included A-I, PV, and cortex ventral and caudal to R. Callosal connections were with R, A-I, PV, and cortex ventral and caudal to R. Callosal connections were with R, A-I, PV, and other locations in temporal cortex. Cortex in caudal PV, ventral to A-I, and ventral to R was responsive to auditory stimuli, but responses to pure tones were weak and inconsistent, and habituation to a repeated stimulus was rapid. The cortex responsive to auditory stimuli included some but not all of the cortex connected with A-I and R. The results lead to the conclusion that auditory cortex of squirrels contains at least two tonotopically organized fields, possibly as many as five or more auditory fields, and at least two auditory-somatosensory fields.

Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields

The responses of neuronal clusters to amplitude-modulated tones were studied in five auditory cortical fields of the anesthetized cat: the primary auditory field (AI), second auditory field (AII), anterior auditory field (AAF), posterior auditory field (PAF) and the ventro-posterior auditory field (VPAF). Modulation transfer functions (MTFs) for amplitude-modulated tones were obtained at 172 cortical locations. MTFs were constructed by measuring firing rate (rate-MTFs) and response synchronization (synchronization-MTFs) to sinusoidal and rectangular waveform modulation of CF-tones. The MTFs were characterized by their ‘best-modulation frequency’ (BMF) and a measure of their quality or ‘sharpness’ ( Q 2 dB ). These characteristics were compared for the five fields. Rate and synchronization MTFs for sinusoidal and rectangular modulation produced similar estimates of BMF and ( Q 2 dB ). Comparison of averaged BMFs between the cortical fields revealed relatively high BMFs in AAF (mean: 31.1 Hz for synchronization to sinusoidal AM) and moderately high BMFs in AI (14.2 Hz) whereas BMFs encountered in AII. VPAF and PAF were generally low (7.0, 5.2, and 6.8 Hz). The MTFs were relatively broadly tuned (low Q 2 dB ) in AAF and sharper in a low modulation group containing AII, PAF and VPAF. The ventro-posterior field was the most sensitive to changes in the modulation waveform. We conclude that there are significant differences between auditory cortical fields with respect to their temporal response characteristics and that the assessment of these response characteristics reveals important aspects of the functional significance of auditory cortical fields for the coding and representation of complex sounds.

Maps of auditory cortex in cats reared after unilateral cochlear ablation in the neonatal period

The responses of many neurons recorded in the high best-frequency region of primary auditory cortical field, AI, of the normal adult cat depend upon intensity differences of the sounds arriving at the two ears. These binaural interactions are exhibited early in postnatal life, well before structural maturation of the auditory pathways from the ear to the cortex is complete. The aim of the present work was to study certain aspects of the functional development of the auditory cortex in adult cats unilaterally deaf from birth. In adult animals reared with a neonatal cochlear ablation, field AI ipsilateral to the non-operated ear showed a normal tonotopic map, which was derived from single neurons and neuron clusters driven securely by best-frequency tonal stimulation in virtually every electrode penetration. The acoustic thresholds at many recording sites were as low as those obtained in AI contralateral to the non-operated ear. These findings are in marked contrast to those from control experiments on normal adult cats where only about 65% of AI neurons were excited by a sound delivered to the ipsilateral ear and where thresholds to ipsilateral ear stimulation were significantly higher than contralateral thresholds. The spatial distribution of cortical neurons based on acoustic thresholds also appeared to be different in cats unilaterally deaf from birth when compared to control cats. Closely spaced electrode penetrations in AI ipsilateral to the non-operated ear suggested that neurons were separated into low-threshold regions and high-threshold regions. There was no evidence for this type of non-random segregation in control experiments.