Macaque Auditory Cortex Research Articles

Dual Time Scales for Categorical Decision Making in Auditory Cortex

Category formation allows us to group perceptual objects into meaningful classes and is fundamental to cognition. Categories can be derived from similarity relationships of object features by using prototypes or multiple exemplars, or from abstract relationships of features and rules . A variety of brain areas have been implicated in categorization processes, but mechanistic insights on the single-cell and local-network level are still rare and limited to the matching of individual objects to categories . For directional categorization of tone steps, as in melody recognition , abstract relationships between sequential events (higher or lower in frequency) have to be formed. To explore the neuronal mechanisms of this categorical identification of step direction, we trained monkeys for more than two years on a contour-discrimination task with multiple tone sequences. In the auditory cortex of these highly trained monkeys, we identified two interrelated types of neuronal firing: Increased phasic responses to tones categorically represented the reward-predicting downward frequency steps and not upward steps; subsequently, slow modulations of tonic firing predicted the behavioral decisions of the monkeys, including errors. Our results on neuronal mechanisms of categorical stimulus identification and of decision making attribute a cognitive role to auditory cortex, in addition to its role in signal processing.

Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex

Anatomical studies propose that the primate auditory cortex contains more fields than have actually been functionally confirmed or described. Spatially resolved functional magnetic resonance imaging (fMRI) with carefully designed acoustical stimulation could be ideally suited to extend our understanding of the processing within these fields. However, after numerous experiments in humans, many auditory fields remain poorly characterized. Imaging the macaque monkey is of particular interest as these species have a richer set of anatomical and neurophysiological data to clarify the source of the imaged activity. We functionally mapped the auditory cortex of behaving and of anesthetized macaque monkeys with high resolution fMRI. By optimizing our imaging and stimulation procedures, we obtained robust activity throughout auditory cortex using tonal and band-passed noise sounds. Then, by varying the frequency content of the sounds, spatially specific activity patterns were observed over this region. As a result, the activity patterns could be assigned to many auditory cortical fields, including those whose functional properties were previously undescribed. The results provide an extensive functional tessellation of the macaque auditory cortex and suggest that 11 fields contain neurons tuned for the frequency of sounds. This study provides functional support for a model where three fields in primary auditory cortex are surrounded by eight neighboring “belt” fields in non-primary auditory cortex. The findings can now guide neurophysiological recordings in the monkey to expand our understanding of the processing within these fields. Additionally, this work will improve fMRI investigations of the human auditory cortex.

Timing of pure tone and noise-evoked responses in macaque auditory cortex

We compared onset latencies for characteristic frequency pure tone and broadband noise responses in AI and posterior belt regions of the auditory cortex in awake macaques. We found that (1) in AI, responses to characteristic frequency tones and broadband noise have similar latencies, (2) in belt regions, characteristic frequency tone and broadband noise latencies differ significantly; broadband noise latencies are shorter, while characteristic frequency tone latencies are longer than corresponding values in AI, (3) for both pure tone and broadband noise responses in AI, latency decreases with increasing characteristic frequency and (4) despite a similar inverse relationship of tone latency and local characteristic frequency in belt areas, broadband noise latencies are uniformly short, and appear unrelated to local characteristic frequency. Dissociation of broadband noise and pure tone latencies may reflect the use of parallel anatomical routes into belt regions.

Auditory Cortical Neurons Respond to Somatosensory Stimulation

The prevailing hierarchical model of cortical sensory processing holds that early processing is specific to individual modalities and that combination of information from different modalities is deferred until higher-order stages of processing. In this paper, we present physiological evidence of multisensory convergence at an early stage of cortical auditory processing. We used multi-neuron cluster recordings, along with a limited sample of single-unit recordings, to determine whether neurons in the macaque auditory cortex respond to cutaneous stimulation. We found coextensive cutaneous and auditory responses in caudomedial auditory cortex, an area lying adjacent to A1, and at the second stage of the auditory cortical hierarchy. Somatosensory-auditory convergence in auditory cortex may underlie effects observed in human studies. Convergence of inputs from different sensory modalities at very early stages of cortical sensory processing has important implications for both our developing understanding of multisensory processing and established views of unisensory processing.

Somatosensory input to auditory association cortex in the macaque monkey.

We investigated the convergence of somatosensory and auditory inputs in within subregions of macaque auditory cortex. Laminar current source density and multiunit activity profiles were sampled with linear array multielectrodes during penetrations of the posterior superior temporal plane in three macaque monkeys. At each recording site, auditory responses to binaural clicks, pure tones, and band-passed noise, all presented by earphones, were compared with somatosensory responses evoked by contralateral median nerve stimulation. Subjects were awake but were not required to discriminate the stimuli. Borders between A1 and surrounding belt regions were identified by mapping best frequency and stimulus preferences and by subsequent histological analysis. Regions immediately caudomedial to A1 had robust somatosensory responses co-represented with auditory responses. In these regions, both somatosensory and auditory response profiles had "feedforward" patterns; initial excitation beginning in Lamina 4 and spreading to extragranular laminae. Auditory and somatosensory responses displayed a high degree of temporal overlap. Anatomical reconstruction indicated that the somatosensory input region includes, but may not be restricted to, the caudomedial auditory association cortex. As was earlier reported for this region, auditory frequency tuning curves were broad and band-passed noise responses were larger than pure tone responses. No somatosensory responses were observed in A1. These findings suggest a potential neural substrate for multisensory integration at an early stage of auditory cortical processing.

Neuronal mechanisms of auditory backward recognition masking in macaque auditory cortex.

The sensation of a single sound event can be altered by subsequent sounds. This study searched for neural mechanisms of such retroactive effects in macaque auditory cortex by comparing neural responses to single tones with responses to two consecutive tones. Retroactive influences were found to affect late parts of the response to a tone, which comprised 53/134 of the recordings of action potentials and 88/131 of the recordings of field potentials performed in primary, caudal, and medial auditory fields. If before or during the occurrence of the late response to the first tone a second tone was presented the late response was suppressed. Suppression of late cortical responses parallels perceptual phenomena like backward recognition masking, suggesting that suppression of late responses provides a neural correlate of auditory backward effects.

Processing of Complex Sounds in the Auditory Cortex of Cat, Monkey, and Man

One of the fundamental features in the organization of sensory cortices which has emerged from 30 years of research in the visual system is the existence of multiple representations of the sensory world in the cerebral cortex. Compared with the visual system much less information exists about the functional specialization of multiple maps in the central auditory system. This is surprising, since an understanding of central auditory representations seems necessary for an understanding of higher auditory processing, including the perception of speech and the perception of auditory space. We have recorded single neuron activity in higher areas of auditory cortex of cats and rhesus monkeys. In cats, activity was recorded in the caudal part of the anterior ectosylvian (AE) cortex (areas AEA and AAF). More than half of the neurons were clearly tuned to the location of a sound source in azimuth and elevation. Frequency-modulated (FM) sounds elicited best responses at fast rates of modulation. By contrast, neurons in the posterior ectosylvian (PE) areas (PAF, VPAF) responded better to slow FM rates. This suggests a possible specialization for the processing of spatial attributes in the AE cortex, and a possible preference for auditory “patterns” in PE. In macaque monkeys, we explored the question of parallel processing in the higher auditory pathways by combining lesion and anatomical tracer techniques with single unit recording. Inactivation of primary auditory cortex (AI) abolished pure-tone responses in the caudomedial area (CM), but not in the rostral area (R). Injections of retrograde fluorescent tracers into R showed strong labeling of the main, ventral nucleus of the medial geniculate (MGv). Both findings suggest the existence of parallel pathways in the auditory cortex, originating at more peripheral sites and possibly specialized for the processing of auditory space vs. auditory patterns. The auditory pattern pathway in Macaque auditory cortex was further explored by using complex stimuli including Macaque-specific communication sounds. Neurons in the lateral belt areas (AL, ML, and CL) respond very selectively to bandpassed noise stimuli, to FM sounds of a certain rate and direction, as well as to certain classes of monkey calls. We are now in the process of exploring higher areas of human auditory cortex by measuring cortical activation with noninvasive functional magnetic resonance imaging (fMRI) while stimulating with complex auditory sounds.

The Role of Macaque Auditory Cortex in Sound Localization

Bilateral ablation of auditory cortex in macaques results in both sensory and perceptual deficits. The sensory deficit is indicated by increased thresholds for left-right locus discriminations and an inability to discriminate locus within either the left or right hemifield. The perceptual deficit is indicated by the observation that the monkeys no longer appear to associate a sound with a location in space. Unilateral auditory cortex ablation results in an inability to discriminate locus within the hemifield contralateral to the lesion. It is not known whether unilateral lesions also result in a perceptual deficit.

Processing of complex sounds in rhesus monkey auditory cortex

Several auditory fields surrounding primary auditory cortex (AI) have been described in the rhesus monkey. Most recently, three areas have been identified in the so-called auditory belt region on the lateral surface of the superior temporal gyrus [Rauschecker et al., Science (1995) (in press)]. Functional identification of these lateral areas (AL, ML, and CL) was based on single unit responses to bandpassed noise (BPN) bursts, which constitute a class of superior stimuli for neurons in this region. Best center frequency (BFc) of the BPN bursts varies systematically along a rostro-caudal axis, revealing three cochleotopic maps. Neurons in the lateral areas also display tuning to a ‘‘best bandwidth’’ of the noise bursts, which varies along a medio-lateral axis, orthogonal to the BFc axis. Digitized vocalizations from the rhesus monkeys’ own repertoire were finally used for presentation during single-unit recording. In many instances, neurons responded even better to the monkey calls than to noise bursts or other synthetic stimuli. It appears that the lateral belt areas of macaque auditory cortex could form an important step in the preprocessing of species-specific communication sounds, somewhat equivalent to superior temporal areas in humans that have been implicated in phonological processing.

Dependence of auditory cortex evoked unit activity on interstimulus interval in the cat.

Dependence of auditory cortex evoked unit activity on interstimulus interval in the cat.S Hocherman, and E GilatS Hocherman, and E GilatPublished Online:01 Jun 1981https://doi.org/10.1152/jn.1981.45.6.987MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByLong-Lasting Context Dependence Constrains Neural Encoding Models in Rodent Auditory CortexHiroki Asari, and Anthony M. Zador1 November 2009 | Journal of Neurophysiology, Vol. 102, No. 5Long-Lasting Modulation by Stimulus Context in Primate Auditory CortexEdward L. Bartlett, and Xiaoqin Wang1 July 2005 | Journal of Neurophysiology, Vol. 94, No. 1Time course of loudness recalibration: Implications for loudness enhancementThe Journal of the Acoustical Society of America, Vol. 114, No. 3Spectral interactions, but no mismatch negativity, in auditory cortex of anesthetized ratHearing Research, Vol. 181, No. 1-2Spontaneous and Stimulus-Evoked Intrinsic Optical Signals in Primary Auditory Cortex of the CatMatthew W. Spitzer, Michael B. Calford, Janine C. Clarey, John D. Pettigrew, and Anna W. Roe1 March 2001 | Journal of Neurophysiology, Vol. 85, No. 3Directional Sensitivity of Neurons in the Primary Auditory (AI) Cortex of the Cat to Successive Sounds Ordered in Time and SpaceRichard A. Reale, and John F. Brugge1 July 2000 | Journal of Neurophysiology, Vol. 84, No. 1Processing of Sound Sequences in Macaque Auditory Cortex: Response EnhancementMichael Brosch, Andreas Schulz, and Henning Scheich1 September 1999 | Journal of Neurophysiology, Vol. 82, No. 3Time Course of Forward Masking Tuning Curves in Cat Primary Auditory CortexMichael Brosch, and Christoph E. Schreiner1 February 1997 | Journal of Neurophysiology, Vol. 77, No. 2The influence of temporal pattern of stimulation on delay tuning of neurons in the auditory cortex of the FM bat, Myotis lucifugusHearing Research, Vol. 66, No. 1Periodicity coding in the auditory systemHearing Research, Vol. 60, No. 2Neural coding of speech sound in the telencephalic auditory area of the mynah birdJournal of Comparative Physiology A, Vol. 169, No. 2Reactions of human auditory cortex to a change in tone durationHearing Research, Vol. 41, No. 1Evoked responses of human auditory cortex may be enhanced by preceding stimuliElectroencephalography and Clinical Neurophysiology/Evoked Potentials Section, Vol. 74, No. 3Neuromagnetic responses of human auditory cortex to interruptions in a steady rhythmNeuroscience Letters, Vol. 99, No. 1-2Responses of single auditory cortical neurons to tone sequencesBrain Research, Vol. 481, No. 1The influence of stimulus repetition on the acoustic startle response and on responses of inferior colliculus neurons of miceBrain Research, Vol. 386, No. 1-2Single unit activity in the auditory cortex and the medial geniculate body of the rhesus monkey: Behavioral modulationBrain Research, Vol. 324, No. 2 More from this issue > Volume 45Issue 6June 1981Pages 987-97 https://doi.org/10.1152/jn.1981.45.6.987PubMed7252536History Published online 1 June 1981 Published in print 1 June 1981 Metrics

An ablation study of the auditory cortex in the cat using binaural tonal patterns.

An ablation study of the auditory cortex in the cat using binaural tonal patterns.J Kaas, S Axelrod, and I T DiamondJ Kaas, S Axelrod, and I T DiamondPublished Online:01 Jul 1967https://doi.org/10.1152/jn.1967.30.4.710MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited BySound sequence discrimination learning is dependent on cholinergic inputs to the rat auditory cortexNeuroscience Research, Vol. 50, No. 1Processing of Sound Sequences in Macaque Auditory Cortex: Response EnhancementMichael Brosch, Andreas Schulz, and Henning Scheich1 September 1999 | Journal of Neurophysiology, Vol. 82, No. 3Time Course of Forward Masking Tuning Curves in Cat Primary Auditory CortexMichael Brosch, and Christoph E. Schreiner1 February 1997 | Journal of Neurophysiology, Vol. 77, No. 2The Brain and Hearing: Auditory Discriminations Affected by Brain Lesions29 June 2016 | Annals of Otology, Rhinology & Laryngology, Vol. 86, No. 4Role of neocortex in binaural hearing in the cat. I. Contralateral maskingBrain Research, Vol. 100, No. 2Some results of studies on split brainPhysiology & Behavior, Vol. 7, No. 5The effects of forebrain commissurotomies on the rate of learning a dark-light discrimination by catsBrain Research, Vol. 14, No. 3Interhemispheric fiber connections of the auditory cortex of the catBrain Research, Vol. 11, No. 1 More from this issue > Volume 30Issue 4July 1967Pages 710-24 https://doi.org/10.1152/jn.1967.30.4.710PubMed6035689History Published online 1 July 1967 Published in print 1 July 1967 Metrics

Tonal discrimination after ablation of auditory cortex.

ArticlesTONAL DISCRIMINATION AFTER ABLATION OF AUDITORY CORTEXIrving T. Diamond, Jay M. Goldberg, and William D. NeffIrving T. Diamond, Jay M. Goldberg, and William D. NeffPublished Online:01 Mar 1962https://doi.org/10.1152/jn.1962.25.2.223MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformationCited ByComparison of Midbrain and Thalamic Space-Specific Neurons in Barn OwlsMaría Lucía Pérez, and José Luis Peña1 February 2006 | Journal of Neurophysiology, Vol. 95, No. 2Sound sequence discrimination learning is dependent on cholinergic inputs to the rat auditory cortexNeuroscience Research, Vol. 50, No. 1Processing of Sound Sequences in Macaque Auditory Cortex: Response EnhancementMichael Brosch, Andreas Schulz, and Henning Scheich1 September 1999 | Journal of Neurophysiology, Vol. 82, No. 3Time Course of Forward Masking Tuning Curves in Cat Primary Auditory CortexMichael Brosch, and Christoph E. Schreiner1 February 1997 | Journal of Neurophysiology, Vol. 77, No. 2Auditory perception of temporal and spectral events in patients with focal left and right cerebral lesionsBrain and Language, Vol. 39, No. 4Psychic ageusia in rats lacking gustatory neocortexExperimental Neurology, Vol. 72, No. 3Sequential auditory and visual discriminations after temporal lobe ablation in monkeysPhysiology & Behavior, Vol. 24, No. 6Duration Discrimination in the Rat after Early Auditory Restriction2 November 2016 | Perceptual and Motor Skills, Vol. 25, No. 1 More from this issue > Volume 25Issue 2March 1962Pages 223-235 https://doi.org/10.1152/jn.1962.25.2.223PubMed13886108History Published online 1 March 1962 Published in print 1 March 1962 Metrics

Ablation of temporal cortex and discrimination of auditory patterns.

ArticlesABLATION OF TEMPORAL CORTEX AND DISCRIMINATION OF AUDITORY PATTERNSIrving T. Diamond, and W. D. NeffIrving T. Diamond, and W. D. NeffPublished Online:01 May 1957https://doi.org/10.1152/jn.1957.20.3.300MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformation Cited ByEarly Stages of Melody Processing: Stimulus-Sequence and Task-Dependent Neuronal Activity in Monkey Auditory Cortical Fields A1 and RPingbo Yin, Mortimer Mishkin, Mitchell Sutter, and Jonathan B. Fritz1 December 2008 | Journal of Neurophysiology, Vol. 100, No. 6Single-Neuron Responses to Rapidly Presented Temporal Sequences in the Primary Auditory Cortex of the Awake Macaque MonkeyM. L. Phan, and G. H. Recanzone1 February 2007 | Journal of Neurophysiology, Vol. 97, No. 2Comparison of Midbrain and Thalamic Space-Specific Neurons in Barn OwlsMaría Lucía Pérez, and José Luis Peña1 February 2006 | Journal of Neurophysiology, Vol. 95, No. 2Sound sequence discrimination learning is dependent on cholinergic inputs to the rat auditory cortexNeuroscience Research, Vol. 50, No. 1Processing of Sound Sequences in Macaque Auditory Cortex: Response EnhancementMichael Brosch, Andreas Schulz, and Henning Scheich1 September 1999 | Journal of Neurophysiology, Vol. 82, No. 3Time Course of Forward Masking Tuning Curves in Cat Primary Auditory CortexMichael Brosch, and Christoph E. Schreiner1 February 1997 | Journal of Neurophysiology, Vol. 77, No. 2Neural coding of speech sound in the telencephalic auditory area of the mynah birdJournal of Comparative Physiology A, Vol. 169, No. 2Auditory perception of temporal and spectral events in patients with focal left and right cerebral lesionsBrain and Language, Vol. 39, No. 4Central action of endogenous sugar acid (2-buten-4-olide): Comparison with local anesthesia in hypothalamusBrain Research Bulletin, Vol. 24, No. 6Characteristics of rat lateral hypothalamic neuron responses to smell and taste in emotional behaviorBrain Research, Vol. 491, No. 1Neuromagnetic responses of human auditory cortex to interruptions in a steady rhythmNeuroscience Letters, Vol. 99, No. 1-2Responses of single auditory cortical neurons to tone sequencesBrain Research, Vol. 481, No. 1Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fieldsHearing Research, Vol. 32, No. 1Age-related changes in auditory temporal perceptionJournal of Experimental Child Psychology, Vol. 44, No. 3Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF)Hearing Research, Vol. 21, No. 3The effects of stimulation of substantia innominata and sensory receiving areas of the forebrain upon the activity of neurons within the amygdala of the anesthetized catBrain Research, Vol. 269, No. 1Encoding of alternating acoustical signals in the medial geniculate body of guinea pigsHearing Research, Vol. 3, No. 4Cortical deafnessJournal of the Neurological Sciences, Vol. 48, No. 1Sequential auditory and visual discriminations after temporal lobe ablation in monkeysPhysiology & Behavior, Vol. 24, No. 6Temporal pattern discrimination survives simultaneous bilateral ablation of suprasylvian cortex but not sequential bilateral ablation of insular-temporal cortex in the catBrain Research, Vol. 173, No. 2Effects of auditory cortex lesions on temporal summation in catsBrain Research, Vol. 136, No. 3Prefrontal granular cortex of the rhesus monkey. I. Intrahemispheric cortical afferentsBrain Research, Vol. 132, No. 2The Brain and Hearing: Auditory Discriminations Affected by Brain Lesions29 June 2016 | Annals of Otology, Rhinology & Laryngology, Vol. 86, No. 4Effect of auditory neocortex ablation on identification of click rates in catsBrain Research, Vol. 116, No. 1A microelectrode study of amygdaloid afferents: Temporal neocortical inputsBrain Research, Vol. 105, No. 3Some variables in auditory pattern discrimination learningNeuropsychologia, Vol. 14, No. 2Auditory and visual discrimination following lesions of the anterior supratemporal plane in monkeysNeuropsychologia, Vol. 14, No. 2Etude psychoacoustique d'un cas de “surdite corticale”Neuropsychologia, Vol. 13, No. 2Polysensory cortical lesions and auditory temporal pattern discriminations in the catBrain Research, Vol. 80, No. 2Insular-temporal lesions and vibrotactile temporal pattern discrimination in catsPhysiology & Behavior, Vol. 12, No. 2The effects of insular and temporal lesions in cats on two types of auditory pattern discriminationBrain Research, Vol. 62, No. 1Responses of single units in the primary auditory cortex of the cat to tones and to tone pairsBrain Research, Vol. 42, No. 2Auditory cortical lesions and visual pattern discrimination in catBrain Research, Vol. 39, No. 2Thalam-Cortical Organization of the Auditory System in the CatProceedings of the Japan Academy, Vol. 48, No. 8Neural structures mediating differential sound intensity discrimination in the catBrain Research, Vol. 27, No. 2Effects of ablations of temporal cortex upon speech sound discrimination in the monkeyExperimental Neurology, Vol. 24, No. 4Duration Discrimination in the Rat after Early Auditory Restriction2 November 2016 | Perceptual and Motor Skills, Vol. 25, No. 1Temporal conditioning of the arousal responsePhysiology & Behavior, Vol. 2, No. 1Auditory organization of the inferior colliculi in the catExperimental Neurology, Vol. 6, No. 6 More from this issue > Volume 20Issue 3May 1957Pages 300-315 https://doi.org/10.1152/jn.1957.20.3.300PubMed13429392History Published online 1 May 1957 Published in print 1 May 1957 Metrics