The representation of heart contractions in some auditory parts of the temporal cortex in a non-anesthetized cat

Although the contributions of primary auditory cortex (AI) to sound localization have been extensively studied in a large number of mammals, little is known of the contributions of nonprimary auditory cortex to sound localization. Therefore the purpose of this study was to examine the contributions of both primary and all the recognized regions of acoustically responsive nonprimary auditory cortex to sound localization during both bilateral and unilateral reversible deactivation. The cats learned to make an orienting response (head movement and approach) to a 100-ms broad-band noise stimulus emitted from a central speaker or one of 12 peripheral sites (located in front of the animal, from left 90 degrees to right 90 degrees , at 15 degrees intervals) along the horizontal plane after attending to a central visual stimulus. Twenty-one cats had one or two bilateral pairs of cryoloops chronically implanted over one of ten regions of auditory cortex. We examined AI [which included the dorsal zone (DZ)], the three other tonotopic fields [anterior auditory field (AAF), posterior auditory field (PAF), ventral posterior auditory field (VPAF)], as well as six nontonotopic regions that included second auditory cortex (AII), the anterior ectosylvian sulcus (AES), the insular (IN) region, the temporal (T) region [which included the ventral auditory field (VAF)], the dorsal posterior ectosylvian (dPE) gyrus [which included the intermediate posterior ectosylvian (iPE) gyrus], and the ventral posterior ectosylvian (vPE) gyrus. In accord with earlier studies, unilateral deactivation of AI/DZ caused sound localization deficits in the contralateral field. Bilateral deactivation of AI/DZ resulted in bilateral sound localization deficits throughout the 180 degrees field examined. Of the three other tonotopically organized fields, only deactivation of PAF resulted in sound localization deficits. These deficits were virtually identical to the unilateral and bilateral deactivation results obtained during AI/DZ deactivation. Of the six nontonotopic regions examined, only deactivation of AES resulted in sound localization deficits in the contralateral hemifield during unilateral deactivation. Although bilateral deactivation of AI/DZ, PAF, or AES resulted in profound sound localization deficits throughout the entire field, the cats were generally able to orient toward the hemifield that contained the acoustic stimulus, but not accurately identify the location of the stimulus. Neither unilateral nor bilateral deactivation of areas AAF, VPAF, AII, IN, T, dPE, nor vPE had any effect on the sound localization task. Finally, bilateral heterotopic deactivations of AI/DZ, PAF, or AES yielded deficits that were as profound as bilateral homotopic cooling of any of these sites. The fact that deactivation of any one region (AI/DZ, PAF, or AES) was sufficient to produce a deficit indicated that normal function of all three regions was necessary for normal sound localization. Neither unilateral nor bilateral deactivation of AI/DZ, PAF, or AES affected the accurate localization of a visual target. The results suggest that hemispheric deactivations contribute independently to sound localization deficits.

The contribution of auditory cortex to spatial information processing was explored behaviourally in adult ferrets by reversibly deactivating different cortical areas by subdural placement of a polymer that released the GABAA agonist muscimol over a period of weeks. The spatial extent and time course of cortical inactivation were determined electrophysiologically. Muscimol-Elvax was placed bilaterally over the anterior (AEG), middle (MEG) or posterior ectosylvian gyrus (PEG), so that different regions of the auditory cortex could be deactivated in different cases. Sound localization accuracy in the horizontal plane was assessed by measuring both the initial head orienting and approach-to-target responses made by the animals. Head orienting behaviour was unaffected by silencing any region of the auditory cortex, whereas the accuracy of approach-to-target responses to brief sounds (40 ms noise bursts) was reduced by muscimol-Elvax but not by drug-free implants. Modest but significant localization impairments were observed after deactivating the MEG, AEG or PEG, although the largest deficits were produced in animals in which the MEG, where the primary auditory fields are located, was silenced. We also examined experience-induced spatial plasticity by reversibly plugging one ear. In control animals, localization accuracy for both approach-to-target and head orienting responses was initially impaired by monaural occlusion, but recovered with training over the next few days. Deactivating any part of the auditory cortex resulted in less complete recovery than in controls, with the largest deficits observed after silencing the higher-level cortical areas in the AEG and PEG. Although suggesting that each region of auditory cortex contributes to spatial learning, differences in the localization deficits and degree of adaptation between groups imply a regional specialization in the processing of spatial information across the auditory cortex.

In humans, damage to posterior parietal or frontal cortices often induces a severe impairment of the ability to redirect gaze to visual targets introduced into the contralateral field. In cats, unilateral deactivation of the posterior middle suprasylvian (pMS) sulcus in the posterior inferior parietal region also results in an equally severe impairment of visually mediated redirection of gaze. In this study we tested the contributions of the pMS cortex and 14 other cortical regions in mediating redirection of gaze to visual targets in 31 adult cats. Unilateral cooling deactivation of three adjacent regions along the posterior bend of the suprasylvian sulcus (posterior middle suprasylvian sulcus, posterior suprasylvian sulcus, and dorsal posterior ectosylvian gyrus at the confluence of the occipital, parietal, and temporal cortices) eliminated visually mediated redirection of gaze towards stimuli introduced into the contralateral hemifield, while the redirection of gaze toward the ipsilateral hemifield remained highly proficient. Additional cortical loci critical for visually mediated redirection of gaze include the anterior suprasylvian gyrus (lateral area 5, anterior inferior parietal cortex) and medial area 6 in the frontal region. Cooling deactivation of: 1) dorsal or 2) ventral posterior suprasylvian gyrus; 3) ventral posterior ectosylvian gyrus, 4) middle ectosylvian gyrus; 5) anterior or 6) posterior middle suprasylvian gyrus (area 7); 7) anterior middle suprasylvian sulcus; 8) medial area 5; 9) the visual portion of the anterior ectosylvian sulcus (AES); 10) or lateral area 6 were all without impact on the ability to redirect gaze. In summary, we identified a prominent field of cortex at the junction of the temporo-occipito-parietal cortices (regions pMS, dPE, PS), an anterior inferior parietal field (region 5L), and a frontal field (region 6M) that all contribute critically to the ability to redirect gaze to novel stimuli introduced into the visual field during fixation. These loci have several features in common with cortical fields in monkey and human brains that contribute to the visually guided redirection of the head and eyes.

Determining the spatial direction of sound sources is one of the major computations performed by the auditory system. The anterior ectosylvian sulcus (AES) of cat cortex is known to be important for sound localization. However, there are contradicting reports as to the spatial response properties of neurons in AES: whereas some studies found narrowly tuned neurons, others reported mostly spatially widely tuned neurons. We hypothesized that this is the result of a nonhomogenous distribution of the auditory neurons in this area. To test this possibility, we recorded neuronal activity along the AES, together with a sample of neurons from primary auditory cortex (A1) of cats in response to pure tones and to virtual acoustic space stimuli. In all areas, most neurons responded to both types of stimuli. Neurons located in posterior AES (pAES) showed special response properties that distinguished them from neurons in A1 and from neurons in anterior AES (aAES). The proportion of space-selective neurons among auditory neurons was significantly higher in pAES (82%) than in A1 (72%) and in aAES (60%). Furthermore, whereas the large majority of A1 neurons responded preferentially to contralateral sounds, neurons in pAES (and to a lesser extent in aAES) had their spatial selectivity distributed more homogenously. In particular, 28% of the space-selective neurons in pAES had highly modulated frontal receptive fields, against 8% in A1 and 17% in aAES. We conclude that in cats, pAES contains a secondary auditory cortical field which is specialized for spatial processing, in particular for the representation of frontal space.

In a preceding report, we described patterns of thalamic retrograde labeling following 17 tracer deposits on the cat's posterior ectosylvian gyrus and concluded, on the basis of patterns of thalamic connectivity, that the posterior ectosylvian gyrus is composed of three major divisions: a tonotopic auditory zone located anteriorly, a belt of auditory association cortex occupying the gyral crown, and a visual belt located posteriorly. We describe here patterns of transcortical retrograde labeling obtained from tracer deposits in the three zones so defined. Our results indicate that the tonotopic auditory strip is innervated primarily by axons from low-order auditory areas (AAF, AI, P, VP, and V), that the auditory belt receives its strongest input from nontonotopic auditory fields (AII, temporal cortex, and other parts of the auditory belt), and that projections to the visual belt derive primarily from extrastriate visual areas (ALLS, PLLS, DLS, 19, 20, and 21) and from association areas affiliated with the visual system (insular cortex, posterior cingulate gyrus, area 7p, and frontal cortex). We discuss the results in relation to previous systems for parcellating the posterior ectosylvian gyrus of the cat and consider the possibility that divisions of the feline posterior ectosylvian gyrus correspond directly to areas making up the superior temporal gyrus in primates.

We examined the ability of mature cats to accurately orient to, and approach, an acoustic stimulus during unilateral reversible cooling deactivation of primary auditory cortex (AI) or 1 of 18 other cerebral loci. After attending to a central visual stimulus, the cats learned to orient to a 100-ms broad-band, white-noise stimulus emitted from a central speaker or 1 of 12 peripheral sites (at 15 degrees intervals) positioned along the horizontal plane. Twenty-eight cats had two to six cryoloops implanted over multiple cerebral loci. Within auditory cortex, unilateral deactivation of AI, the posterior auditory field (PAF) or the anterior ectosylvian sulcus (AES) resulted in orienting deficits throughout the contralateral field. However, unilateral deactivation of the anterior auditory field, the second auditory cortex, or the ventroposterior auditory field resulted in no deficits on the orienting task. In multisensory cortex, unilateral deactivation of neither ventral or dorsal posterior ectosylvian cortices nor anterior or posterior area 7 resulted in any deficits. No deficits were identified during unilateral cooling of the five visual regions flanking auditory or multisensory cortices: posterior or anterior ii suprasylvian sulcus, posterior suprasylvian sulcus or dorsal or ventral posterior suprasylvian gyrus. In motor cortex, we identified contralateral orienting deficits during unilateral cooling of lateral area 5 (5L) or medial area 6 (6m) but not medial area 5 or lateral area 6. In a control visual-orienting task, areas 5L and 6m also yielded deficits to visual stimuli presented in the contralateral field. Thus the sound-localization deficits identified during unilateral deactivation of area 5L or 6m were not unimodal and are most likely the result of motor rather than perceptual impairments. Overall, three regions in auditory cortex (AI, PAF, AES) are critical for accurate sound localization as assessed by orienting.

1. Physiological methods were used to examine the pattern of inputs from different sensory cortices onto individual superior colliculus neurons. 2. Visual, auditory, and somatosensory influences from anterior ectosylvian sulcus (AES) and visual influences from lateral suprasylvian (LS) cortex were found to converge onto individual multisensory neurons in the cat superior colliculus. An excellent topographic relationship was found between the different sensory cortices and their target neurons in the superior colliculus. 3. Corticotectal inputs were derived solely from unimodal neurons. Multisensory neurons in AES and LS were not antidromically activated from the superior colliculus. 4. Orthodromic and antidromic latencies were consistent with monosynaptic corticotectal inputs arising from LS and the three subdivisions of AES (SIV, Field AES, and AEV). 5. Superior colliculus neurons that received convergent cortical inputs formed a principal component of the tecto-reticulospinal tract. Thus there appears to be extensive cortical control over the output neurons through which the superior colliculus mediates attentive and orientation behaviors. 6. Two other multisensory circuits were identified. A population of multisensory superior colliculus neurons was found, which neither received convergent cortical input nor projected into the tecto-reticulo-spinal tract. In addition, multisensory neurons in AES and LS proved to be independent of the superior colliculus (i.e., they were not corticotectal). While it is likely that these three distinct multisensory neural circuits have different functional roles, their constituent neurons appear to integrate their various sensory inputs in much the same way.

Characterizing neuronal responses to natural stimuli remains a central goal in sensory neuroscience. In auditory cortical neurons, the stimulus selectivity of elicited spiking activity is summarized by a spectrotemporal receptive field (STRF) that relates neuronal responses to the stimulus spectrogram. Though effective in characterizing primary auditory cortical responses, STRFs of non-primary auditory neurons can be quite intricate, reflecting their mixed selectivity. The complexity of non-primary STRFs hence impedes understanding how acoustic stimulus representations are transformed along the auditory pathway. Here, we focus on the relationship between ferret primary auditory cortex (A1) and a secondary region, dorsal posterior ectosylvian gyrus (PEG). We propose estimating receptive fields in PEG with respect to a well-established high-dimensional computational model of primary-cortical stimulus representations. These "cortical receptive fields" (CortRF) are estimated greedily to identify the salient primary-cortical features modulating spiking responses and in turn related to corresponding spectrotemporal features. Hence, they provide biologically plausible hierarchical decompositions of STRFs in PEG. Such CortRF analysis was applied to PEG neuronal responses to speech and temporally orthogonal ripple combination (TORC) stimuli and, for comparison, to A1 neuronal responses. CortRFs of PEG neurons captured their selectivity to more complex spectrotemporal features than A1 neurons; moreover, CortRF models were more predictive of PEG (but not A1) responses to speech. Our results thus suggest that secondary-cortical stimulus representations can be computed as sparse combinations of primary-cortical features that facilitate encoding natural stimuli. Thus, by adding the primary-cortical representation, we can account for PEG single-unit responses to natural sounds better than bypassing it and considering as input the auditory spectrogram. These results confirm with explicit details the presumed hierarchical organization of the auditory cortex.

Auditory Brain Development in Children With Hearing Loss – Part One

Corticothalamic and corticotectal projections from the anterior ectosylvian sulcus (AES) in neonatal cats were studied with anterograde and retrograde neuroanatomical techniques. When the injection site was relatively restricted to the sulcal walls and fundus of the rostral AES (i.e., the SIV cortex), heavy ipsilateral thalamic label was observed in the medial subdivision of the posterior group, in the suprageniculate nucleus, and in the external medullary lamina. No terminal label was seen in the contralateral thalamus although the contralateral homotopic cortex was heavily labeled. Within the ventrobasal complex (VB), dense axonal label was observed in fascicles that traversed VB, but only light terminal label was observed within VB itself. However, in cases where the tracer spread into adjacent SII, terminal label in VB was pronounced. Similarly, when the injection site extended into auditory cortex, terminal label was observed in the lateral and intermediate subdivisions of the posterior group. Rostral AES injections produced distinct, predominantly ipsilateral, terminal label in the superior colliculus that was distributed in two tiers: a discontinuous band in the stratum griseum intermedium and a more diffuse band in stratum griseum profundum. Caudally, dense terminal label was seen in the intercollicular zone and dorsolateral periaqueductal gray. When the injection site did not include rostral AES, no label was observed in the superior colliculus. Horseradish peroxidase injections into the superior colliculus of neonates produced retrogradely labeled neurons throughout the AES, but none was found on the crown of the gyrus where SII is located. Thus, the neonatal corticotectal somatosensory projection arises exclusively from AES and parallels that found in adults. These data indicate that the elaboration of a major descending somatosensory pathway from AES to the thalamus and midbrain is largely a prenatal event. The in utero anatomical maturation of the corticofugal projections from SIV cortex to the superior colliculus contrasts with the protracted postnatal development of the corticotrigeminal projections from SI cortex but is consistent with the mature anatomical state of ascending trigeminotectal projections.

Physiological and behavioral studies in cat have shown that corticotectal influences play important roles in the information-processing capabilities of superior colliculus (SC) neurons. While corticotectal inputs from the anterior ectosylvian sulcus (AES) play a comparatively small role in the unimodal responses of SC neurons, they are particularly important in rendering these neurons capable of integrating information from different sensory modalities (e.g., visual and auditory). The present experiments examined the behavioral consequences of depriving SC neurons of AES inputs, and thereby compromising their ability to integrate visual and auditory information. Selective deactivation of a variety of other cortical areas (posterolateral lateral suprasylvian cortex, PLLS; primary auditory cortex, AI; or primary visual cortex, 17/18) served as controls. Cats were trained in a perimetry device to ignore a brief, low-intensity auditory stimulus but to orient toward and approach a nearthreshold visual stimulus (a light-emitting diode, LED) to obtain food. The LED was presented at different eccentricities either alone (unimodal) or combined with the auditory stimulus (multisensory). Subsequent deactivation of the AES, with focal injections of a local anesthetic, had no effect on responses to unimodal cues regardless of their location. However, it profoundly, though reversibly, altered orientation and approach to multisensory stimuli in contralateral space. The characteristic enhancement of these responses observed when an auditory cue was presented in spatial correspondence with the visual stimulus was significantly degraded. Similarly, the inhibitory effect of a spatially disparate auditory cue was significantly ameliorated. The observed effects were specific to AES deactivation, as similar effects were not obtained with deactivation of PLLS, AI or 17/18, or saline injections into the AES. These observations are consistent with postulates that specific cortical-midbrain interactions are essential for the synthesis of multisensory information in the SC, and for the orientation and localization behaviors that depend on this synthesis.

Integration of Bimodal Looming Signals through Neuronal Coherence in the Temporal Lobe

The medial geniculate nucleus (MG) is well known to send projection fibers not only to the auditory cortex, but also to the limbic structures of the forebrain including the perirhinal cortex and amygdala. In the cat, the non-laminated portions of the MG are also known to project to the amygdala, as well as to the auditory cortical areas surrounding the primary auditory area. On the other hand, projections from the non-laminated MG to the limbic cortical areas have not so far been studied systematically. Thus, in the present study, direct projections from the non-laminated portions of the medial geniculate nucleus to the temporal polar cortex and amygdala were examined in the cat by retrograde and anterograde tract-tracing techniques. The temporal polar cortex is the ventral polar region of the posterior sylvian and posterior ectosylvian gyri, which is located dorsal to the posterior rhinal sulcus and includes the ectorhinal area. After injection of cholera toxin B subunit into the temporal polar cortex, retrogradely labeled neurons were seen in the caudal two-thirds of the medial geniculate nucleus ipsilateral to the injection; they were distributed in the non-laminated portions of the MG (the dorsal and medial divisions and the ventromedial part of the ventral division), but not in the laminated portion (the principal part of the ventral division). These findings were confirmed by injecting Phaseolus vulgaris leucoagglutinin into each division of the MG. After the injection into each non-laminated division, terminal labeling was observed in the temporal polar cortex. Terminal labeling was further found in the lateral amygdaloid nucleus ipsilateral to the injection. Then, cholera toxin B subunit was injected into the lateral amygdaloid nucleus; retrogradely labeled neurons were observed ipsilaterally in the non-laminated portions of the MG, as well as in the temporal polar cortex. The results indicate that the non-laminated portions of the MG send projection fibers to the temporal polar cortex and lateral amygdaloid nucleus, and that the non-laminated portions of the MG and temporal polar cortex give rise to overlapping projections to the lateral amygdaloid nucleus. These connections appear to constitute neuronal links in "emotional" and/or "motivational" circuitry in the forebrain.

The organization of sensory representations in the cortex of the anterior ectosylvian sulcus (AES) of the cat was investigated using single-unit recording techniques. Somatic, auditory, and visual cells were found in the AES but were partially segregated. Somatic cells were concentrated in the rostral two-thirds of the sulcus, auditory cells were found in the caudal third, and visual cells were distributed along the fundus. A distinct, heretofore unknown, somatotopic representation of the body surface was observed in the AES and was designated SIV. The representation of the body in SIV extends along a rostrocaudal axis and the entire somatotopic map is inverted, with the head rostral and the hindquarters caudal. The representation of the paws extends over the lip of the sulcus to abut the paw representations in SII, and the SIV-SII boundary is marked by a reversal in the sequence of receptive fields along the AEG-AES. The SIV representation (SII) on the crown of the anterior ectosylvian gyrus (AEG). The somatotopic map in SII was found to extend further lateral on the AEG than shown by some investigations and it contains a double representation of the limbs: a large representation with the limbs having the opposite orientation to and abutting the SIV map and a smaller representation located more medial on the AEG and extending into the suprasylvian sulcus. The presence of this double representation may help to explain previous discrepancies regarding the overall orientation of the body in SII.

Auditory Brain Development in Children with Hearing Loss – Part Two