Functional Organization Of Auditory Cortex Research Articles

A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex.

The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschl's gyrus (HG) with pronounced induced high-frequency (70–150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however, their distribution within auditory cortex has not been established. Alpha activity (7–14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (4 female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function.SIGNIFICANCE STATEMENT To understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7–14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschl's gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations.

Chronometry on Spike-LFP Responses Reveals the Functional Neural Circuitry of Early Auditory Cortex Underlying Sound Processing and Discrimination.

Animals and humans rapidly detect specific features of sounds, but the time courses of the underlying neural response for different stimulus categories is largely unknown. Furthermore, the intricate functional organization of auditory information processing pathways is poorly understood. Here, we computed neuronal response latencies from simultaneously recorded spike trains and local field potentials (LFPs) along the first two stages of cortical sound processing, primary auditory cortex (A1) and lateral belt (LB), of awake, behaving macaques. Two types of response latencies were measured for spike trains as well as LFPs: (1) onset latency, time-locked to onset of external auditory stimuli; and (2) selection latency, time taken from stimulus onset to a selective response to a specific stimulus category. Trial-by-trial LFP onset latencies predominantly reflecting synaptic input arrival typically preceded spike onset latencies, assumed to be representative of neuronal output indicating that both areas may receive input environmental signals and relay the information to the next stage. In A1, simple sounds, such as pure tones (PTs), yielded shorter spike onset latencies compared to complex sounds, such as monkey vocalizations (“Coos”). This trend was reversed in LB, indicating a hierarchical functional organization of auditory cortex in the macaque. LFP selection latencies in A1 were always shorter than those in LB for both PT and Coo reflecting the serial arrival of stimulus-specific information in these areas. Thus, chronometry on spike-LFP signals revealed some of the effective neural circuitry underlying complex sound discrimination.

The Signs of Silence

How does auditory cortex respond to silence? In this issue of Neuron, show that activity in macaque auditory cortex is highly structured even in the absence of sensory stimuli. These data reveal a close link between spontaneous neural activity and the functional organization of auditory cortex.

Organized Representation of Spectrotemporal Features in Songbird Auditory Forebrain

Much of our understanding of the functional organization of auditory cortex is based on relatively simple stimuli, and the cortical representation of complex sounds remains poorly understood. With their rich vocal communication and learning behaviors, songbirds can offer insights into the neural processing of complex acoustic signals analogous to human speech. In the primary forebrain auditory area field L (primary auditory cortex analog) of zebra finches, previous studies identified a limited set of spectrotemporal receptive field (STRF) types, but whether these were spatially organized remained unclear. Here, we investigated the spatial organization of field L in multiple anatomical planes, using multielectrode array recordings and a stimulus that captures aspects of spectrotemporal modulations of song. Our data demonstrate two separate axes along which spectrotemporal aspects of sound are mapped: width of spectral tuning changes systematically from narrow to broad mediolaterally, whereas width of temporal tuning changes markedly, from narrow to broad, from the input to the output layers. These spatial patterns, which are evident in STRFs computed from both multiple and single units, result in a mapping of basic STRF types to subregions of field L. This highly organized representation of spectrotemporal features of sound contrasts with current views of mammalian auditory cortex, where no strong spatial organization of STRF shapes has been seen thus far. Our data identify a coherent initial cortical representation of sound features and suggest that forebrain filtering for basic perceptual qualities of sound occurs in a spatially organized and segregated manner in the songbird auditory system.

Transformation of Temporal Processing Across Auditory Cortex of Awake Macaques

The anatomy and connectivity of the primate auditory cortex has been modeled as a core region receiving direct thalamic input surrounded by a belt of secondary fields. The core contains multiple tonotopic fields (including the primary auditory cortex, AI, and the rostral field, R), but available data only partially address the degree to which those fields are functionally distinct. This report, based on single-unit recordings across four hemispheres in awake macaques, argues that the functional organization of auditory cortex is best understood in terms of temporal processing. Frequency tuning, response threshold, and strength of activation are similar between AI and R, validating their inclusion as a unified core, but the temporal properties of the fields clearly differ. Onset latencies to pure tones are longer in R (median, 33 ms) than in AI (20 ms); moreover, synchronization of spike discharges to dynamic modulations of stimulus amplitude and frequency, similar to those present in macaque and human vocalizations, suggest distinctly different windows of temporal integration in AI (20-30 ms) and R (100 ms). Incorporating data from the adjacent auditory belt reveals that the divergence of temporal properties within the core is in some cases greater than the temporal differences between core and belt.

Task-Dependent Activations of Human Auditory Cortex during Pitch Discrimination and Pitch Memory Tasks

The functional organization of auditory cortex (AC) is still poorly understood. Previous studies suggest segregation of auditory processing streams for spatial and nonspatial information located in the posterior and anterior AC, respectively (Rauschecker and Tian, 2000; Arnott et al., 2004; Lomber and Malhotra, 2008). Furthermore, previous studies have shown that active listening tasks strongly modulate AC activations (Petkov et al., 2004; Fritz et al., 2005; Polley et al., 2006). However, the task dependence of AC activations has not been systematically investigated. In the present study, we applied high-resolution functional magnetic resonance imaging of the AC and adjacent areas to compare activations during pitch discrimination and n-back pitch memory tasks that were varied parametrically in difficulty. We found that anterior AC activations were increased during discrimination but not during memory tasks, while activations in the inferior parietal lobule posterior to the AC were enhanced during memory tasks but not during discrimination. We also found that wide areas of the anterior AC and anterior insula were strongly deactivated during the pitch memory tasks. While these results are consistent with the proposition that the anterior and posterior AC belong to functionally separate auditory processing streams, our results show that this division is present also between tasks using spatially invariant sounds. Together, our results indicate that activations of human AC are strongly dependent on the characteristics of the behavioral task.

Functional imaging of human auditory cortex

This review summarizes recent advances in functional magnetic resonance imaging that reveal similarities in the organization of human auditory cortex (HAC) and auditory cortex of nonhuman primates. Functional magnetic resonance imaging studies have shown that HAC is a compact region that covers less than 8% of the total cortical surface. HAC is subdivided into more than a dozen distinct auditory cortical fields (ACFs) that surround Heschl's gyri on the superior temporal plane. Recent advances that permit the visualization of the results of functional magnetic imaging experiments directly on the cortical surface have provided new insights into the organization of human ACFs. Evidence suggests that medial regions of HAC are organized in a manner similar to the auditory cortex of other primate species with a set of tonotopically organized core ACFs surrounded by belt ACFs that often share tonotopic organization with the core. Although influenced by attention, responses in HAC core and belt fields are largely determined by the acoustic properties of stimuli, including their frequency, intensity, and location. In contrast, lateral regions of HAC contain parabelt fields that are little influenced by simple acoustic features but rather respond to behaviorally relevant complex sounds such as speech and are strongly modulated by attention. HAC conserves the basic structural and functional organization of auditory cortex as seen in old world primate species. A central challenge to future research is to understand how this basic primate plan has evolved to support uniquely human abilities such as music and language.

Coding of FM sweep trains and twitter calls in area CM of marmoset auditory cortex

The primate auditory cortex contains three interconnected regions (core, belt, parabelt), which are further subdivided into discrete areas. The caudomedial area (CM) is one of about seven areas in the belt region that has been the subject of recent anatomical and physiological studies conducted to define the functional organization of auditory cortex. The main goal of the present study was to examine temporal coding in area CM of marmoset monkeys using two related classes of acoustic stimuli: (1) marmoset twitter calls; and (2) frequency-modulated (FM) sweep trains modeled after the twitter call. The FM sweep trains were presented at repetition rates between 1 and 24 Hz, overlapping the natural phrase frequency of the twitter call (6–8 Hz). Multiunit recordings in CM revealed robust phase-locked responses to twitter calls and FM sweep trains. For the latter, phase-locking quantified by vector strength (VS) was best at repetition rates between 2 and 8 Hz, with a mean of about 5 Hz. Temporal response patterns were not strictly phase-locked, but exhibited dynamic features that varied with the repetition rate. To examine these properties, classification of the repetition rate from the temporal response pattern evoked by twitter calls and FM sweep trains was examined by Fisher’s linear discrimination analysis (LDA). Response classification by LDA revealed that information was encoded not only by phase-locking, but also other components of the temporal response pattern. For FM sweep trains, classification was best for repetition rates from 2 to 8 Hz. Thus, the majority of neurons in CM can accurately encode the envelopes of temporally complex stimuli over the behaviorally-relevant range of the twitter call. This suggests that CM could be engaged in processing that requires relatively precise temporal envelope discrimination, and supports the hypothesis that CM is positioned at an early stage of processing in the auditory cortex of primates.

Spectrotemporal Analysis of Evoked and Induced Electroencephalographic Responses in Primary Auditory Cortex (A1) of the Awake Monkey

Electroencephalography is increasingly being used to probe the functional organization of auditory cortex. Modulation of the electroencephalographic (EEG) signal by tones was examined in primary auditory cortex (A1) of awake monkeys. EEG data were measured at 4 laminar depths defined by current source density profiles evoked by best frequency (BF) tones. Midlaminar multiunit activity was used to define the tuning characteristics of A1 sites. Presentation of BF tones increased EEG power across the range of frequencies examined (4-290 Hz), with maximal effects evident within the first 100 ms after stimulus onset. The largest relative increases in EEG power generally occurred at very high gamma frequency bands (130-210 Hz). Increases in EEG power for frequencies less than 70 Hz primarily represented changes in phase-locked activity, whereas increases at higher frequencies primarily represented changes in non-phase-locked activity. Power increases in higher gamma bands were better correlated with the A1 tonotopic organization than power increases in lower frequency bands. Results were similar across the 4 laminar depths examined. These findings highlight the value of examining high-frequency EEG components in exploring the functional organization of auditory cortex and may enhance interpretation of related studies in humans.

Fine functional organization of auditory cortex revealed by Fourier optical imaging

We provide an overall view of the functional tonotopic organization of the auditory cortex in the rat. We apply a recently developed technique for acquiring intrinsic signal optical maps, Fourier imaging, in the rat auditory cortex. These highly detailed maps, derived in a several-minute-long recording procedure, delineate multiple auditory cortical areas and demonstrate their shapes, sizes, and tonotopic order. Beyond the primary auditory cortex, there are at least three distinct areas with fine-scale tonotopic organization, as well as at least one additional high-frequency field. The arrangement of all of these cortical areas is consistent across subjects. The accuracy of these optical maps was confirmed by microelectrode mapping in the same subjects. This imaging method allows fast mapping of the auditory cortex at high spatial resolution comparable to that provided by conventional microelectrode technique. Although spiking activity is largely responsible for the evoked intrinsic signals, certain features of the optical signal cannot be explained by spiking activity only, and should probably be attributed to other mechanisms inducing metabolic activity, such as subthreshold membrane phenomena.

The unexpected consequences of a noisy environment

A recent study found that the functional organization of auditory cortex was disrupted when rats were exposed to a moderate level of continuous noise during early development. However, this detrimental effect on auditory cortex could be remedied later by stimulating the noise-reared rats with structured sounds. These findings suggest that the endpoint of the ‘critical period’ could be extended well into adult life, which has significant implications for our understanding of cortical plasticity.

Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures.

The subcortical connections of the four tonotopically organized fields of the auditory cortex of the Mongolian gerbil, namely the primary (AI), the anterior (AAF), the dorsoposterior (DP) and the ventroposterior field (VP), were studied predominantly by anterograde transport of biocytin injected into these fields. In order to allow the localization of connections with respect to subdivisions of subcortical auditory structures, their cyto-, fibre- and chemoarchitecture was characterized using staining methods for cell bodies, myelin and the calcium-binding protein parvalbumin. Each injected auditory cortical field has substantial and reciprocal connections with each of the three subdivision of the medial geniculate body (MGB), namely the ventral (MGv), dorsal (MGd) and medial division (MGm). However, the relative strengths of these connections vary: AI is predominantly connected with MGv, AAF with MGm and MGv, and DP and VP with MGd and MGv. The connections of at least AI and MGv are topographic: injections into caudal low-frequency AI label laterorostral portions of MGv, whereas injections into rostral high-frequency AI label mediocaudal portions of MGv. All investigated auditory fields send axons to the suprageniculate, posterior limitans, laterodorsal and lateral posterior thalamic nuclei, with strongest projections from DP and VP, as well as to the reticular and subgeniculate thalamic nuclei. AI, AAF, DP and VP project to all three subdivisions of the inferior colliculus, namely the dorsal cortex, external cortex and central nucleus ipsilaterally and to the dorsal and external cortex contralaterally. They also project to the deep and intermediate layers of the ipsilateral superior colliculus, with strongest projections from DP and VP to the lateral and basolateral amygdaloid nuclei, the caudate putamen, globus pallidus and the pontine nuclei. In addition, AAF and particularly DP and VP project to paralemniscal regions around the dorsal nucleus of the lateral lemniscus (DNLL), to the DNLL itself and to the rostroventral aspect of the superior olivary complex. Moreover, DP and VP send axons to the dorsal lateral geniculate nucleus. The differences with respect to the existence and/or relative strengths of subcortical connections of the examined auditory cortical fields suggest a somewhat different function of each of these fields in auditory processing.

Correlations between neural discharges are related to receptive field properties in cat primary auditory cortex.

The functional role of correlated neural activity in auditory cortex for the processing of sounds was explored by investigating whether and how cross-correlation parameters are related to receptive field similarities of neurons. Multi-unit activity was recorded simultaneously from several sites of isofrequency domains in primary auditory cortex. At each site various receptive field properties were determined. From the discharges of pairs of clusters, normalized cross-correlation histograms (CCH) were calculated for extended periods of spontaneous activity and for periods with noise-burst stimulation. In both conditions, most CCHs exhibited a symmetrical positivity near the origin of the CCH, a few to several tens of milliseconds wide. Cross-correlation histograms were characterized with two parameters: the correlation strength, which was estimated from the peak correlation, and the correlation width, i.e. the time period of correlated firing, which was measured as the width of the positivity at half height. It was found that correlation strength increased and correlation width narrowed with increasing similarity of the receptive fields of two clusters. These relationships were observed both in the acoustically-driven and spontaneous conditions. Specifically, correlation strength was most strongly associated with similarity in binaural interaction and in temporal response properties such as response onset, response offset and the temporal pattern of the response. Correlation width was predominantly associated with similarity in characteristic frequency, bandwidth and intensity threshold. Results suggest that correlated activity, reflecting potential mechanisms involved in the neural computation in auditory cortex, provides a means to evaluate the properties of the functional organization of auditory cortex. Systematic relationships were found between correlation properties and the receptive field-based organization of cortical processing, suggesting that similar general mechanisms are utilized in many parts of the sensory cortex. In particular, the magnitude and/or the time period of synchronized firing of neurons is increased if the receptive field properties of the involved neurons are similar.

Cortical processing of complex sounds

Work on the functional organization of auditory cortex in nonhuman primates has recently gained increasing attention. Neurophysiological studies using complex stimuli, combined with anatomical tract tracing, reveal a hierarchy of cortical processing comparable to other sensory systems. On the basis of these findings from animal studies, together with the advent of modern neuroimaging methods used in human cortex, the field of auditory neuroscience could soon arrive at a detailed understanding of the cortical representation of complex sounds, including speech.

Effect of bilateral auditory cortex lesions on absolute thresholds in Japanese macaques

1. The behavioral audiograms of four Japanese macaques (Macaca fuscata) were assessed before and after receiving two-stage bilateral lesions of auditory cortex. Thresholds were assessed for each ear with the use of insertion earphones. 2. The bilateral lesions resulted in a large initial hearing loss followed by partial recovery that left the animals with a permanent hearing loss in both ears. 3. The initial hearing loss consisted of a total insensitivity to sound in the ear contralateral to the second lesion with limited hearing in the other ear. However, the animal with the most complete lesion was initially unable to hear sound in either ear. Broadband noise was often more effective in eliciting a behavioral response than tones. 4. Partial recovery occurred in all animals and was observed as early as the first week after surgery. Most of this recovery occurred during the first 3-7 wk after surgery. This rapid phase of recovery was sometimes followed by a more gradual phase although thresholds were still elevated after 94 wk. 5. The permanent hearing loss, which averaged from 30 to 44 dB, was not constant across frequency. Threshold shifts were smallest at 63 Hz and progressively increased with frequency to a maximum loss from 8 to 25 kHz with slightly less loss at 32 kHz. 6. Analysis of the psychophysical functions and threshold stability gave no indication of any nonsensory deficits in attention or vigilance. 7. These results, taken with those of previous experiments, indicate that each hemisphere is primarily involved in the detection of sound in the contralateral ear and secondarily involved in detection in the ipsilateral ear. This arrangement differs from that seen in sound localization where each hemisphere is involved with the contralateral hemifield as opposed to the contralateral ear. Thus it appears that the functional organization of auditory cortex for sound localization is different from that for the detection and identification of sound itself.