164 Auditory processing in primate cerebral cortex Jon H Kaas*, Troy A Hackett! and Mark Jude Tramo? ‘Auditory information is relayed from the ventral nucleus of the medial geniculate complex to a core of three primary or primary-lke areas of auditory cortex that are cochleotopically, organized and highly responsive to pure tones. Auditory information is then distributed from the core areas to a ‘surrounding belt of about seven areas that are lese precisely cochleotopic and generally more responsive to complex stimuli than tones. Recent studies indicate that the belt areas relay to the rostral and caudal divisions of a parabelt region at a third level of processing in the cortex lateral to the belt. The parabelt ‘and belt regions have additional inputs from dorsal and ‘magnocellular divisions of the madial geniculate complex and ‘ther pars of the thalamus. The belt and parabelt regions appear to be concerned with integrative and associative functions involved in pattern perception and object recognition The parabelt fields connect with regions of temporal, parietal, and frontal cortex that mediate additional aucitory functions, including space perception and auditory memory. Addresses "Deparment of Psychology, Vanderbilt University, 301 Wilson Hall, 111 2161 Avenue South, Nashville, Tennessee 37240, USA ‘ermal jonh kaas@vanderbitedu ‘ermal: toy.ahackent@vanderbilted {Departments of Neurobiology and Neurology, Harvard Medical ‘School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA; ‘emai mirame@hms harvard edu Current Opinion in Neurobiology 1899, 9:164~170 Intp//biomednet.com/elecrel/0959438800900164 © Elsevier Scionce Lid ISSN 0959-4988, Abbreviations A primary auditory cortex AL Antorolateral eld CL Caudoateral fils CM caudomedtal field EP evoked potential MG medial genicuate complex MGd dorsal division of MG NGm medal dison of MG MGy ventral dision of MG ML idle lateral fla R rostral core field RT rostrotemporal field STG superior temporal gyrus TG transverse gyrus of Hoschl Introduction Recent years have witnessed a growing interest in the basic neural mechanisms underlying auditory cortical pro- cessing in primates, This interest has been kindled, in part, by che development of noninvasive techniques for physiological investigations of auditory perception in humans. Because microelectrode recordings in human auditory cortex are possible only under the rarest of cir cums and in viva tracer studies not at all, advances in knowledge about single-unit physiology, connectivity nd physiological-microanatomical correlates are fueled by research in nonhuman primates and other mammals [1, For anatomical [3,4], functional [5,6], and phylogenetic ‘ons, research in macaque auditory cortex may be espe cially relevant to humans Physiological and functional data are best interpreted with- jin an anatomical framework for auditory processing in superior cemporal cortex, We subdivide primate auditory cortex into three areas — the core, belt, and parabelt — on the basis of their cochleotopic organization, connectional relationships, and architectonic features (Figure 1). Rach region includes several subdivisions with parallel connec tions, and each region consticures one stage in a series of connections, Connections of the parabelt with hetero- modal and supramodal regions of cemporal, frontal, and parietal cortex form a distributed neework for audieory cog- nition (Figure 2). ‘This review describes current views of auditory cortical processing in primates based on recent anatomical and physiological studies. Hierarchical and parallel processing in the core, belt, and parabelt Over the past several years, microelectrode recordings, tracer studies, and histochemical analyses (7.89.10, have provided a detailed account of the hierar- chical and parallel organization of macaque auditory cortex. The core até cortex: Koniocellular architecture, dense myelination, and reactivity for oxidase, cholinesterase, and parvalbumin. Initially, much or all of the core area was considered t© be the classical primary auditory field, AL. However, recent studies have revealed, that the core contains three cochleotopically organized, fields, all of which receive dense inputs from the ventral division of the medial geniculate complex (MGv). In AI, the largest, most caudal field, the histological features list- ed above are pronounced, and low-t0-high Frequencies are mapped anterolaterally to posteromedially In the rostrotemporal field (RT), the smallest, most rostral field, the above histological features arc k and low-to-high frequencies are mapped. field, R, which is intermediate to AL and RT in position, size and histological features, has a posterior-to-anterior representation of low-to-high frequencies. This anatomical organization, together with physiological evidence that ablation of AI docs not abolish neuronal pure tone sensi- tivity in R [11**], suggests chat auditory information is processed in series from the MGv to the core and in paral- core fields has histological features of primary sensory dense ‘cytochrome acetyl- st pronounced, The rostral eore lel within che thre: In che human licerature, there exists some variability across studies concerning the prevalence and precise orientation of cochleoropy within the transverse gyrus of Hesch! (TG),‘Auditory processing in primate cerebral cortex Kaas, Hackett and Tiamo 165 Figure 1 Levele and regions of auditory cortical processing. Th lateral sulcus (LS) has been pened 10 show auditory areas ofthe lower bank (upper bank nat shown), and the superioe temporal sulcus (STS) has been ‘pened to show the extension af auditony related cortex into tis sulcus. Levelt represents the core (darkest shading); evel 2 represents the belt (moderate shading) level represents the parabet (ight shading): level 42 represents the temporal region (Gense hatching and level 4b represents the frontal region (sparse hatching) AL, anterolateral: AS, arcuate suleus CL, caudolateral; CS, central sulcus; IPS, intaparietal sulcus; LuS, lnate sulcus; ML, mice lateral: PS, principal sulcus; RRM, rostromedial; RTL, lateral rastrotemporal: RTM, medial rostvotorporal; STGr, rostral supetior temporal gyrus. Based on data roe (126,139,37°38"] 4b Principals ‘4b Medial 4b Arcuate 2 Belt 3 Parabolt A y ‘4a Temporal pian Newsboy wherein koniocortex resides {4]. The current consensus among magnetic and electrical evoked potential (BP) stud- jes [14-16], functional imaging studies (for a review, see [17)}, and a microelectrode study in an epilepyy patient [18] is that low-to-high frequencies are mapped anterolaterally to posteromedially in TG — similar co the orientation found in macaque AL Some EP results [19] and preliminary func~ sional imaging data [17] raise the possibility of two cochlear representations in ‘TG that could constitute the human homologs of macaque AT and R. In macaques and humans, the functional consequences of bilateral lesions involving the core afca orits inputs typically include a profound deficit, in sound detection chat at least partially resolves over months and leaves the listener with trouble perceiving what is heard and where it is coming from [5,20-22]. The belt region, which surrounds the core, does nor exhib- it the histological features of primary sensory cortex and does not receive dense projections from MGv. It receives ‘most of its afferene input from the core area and the dorsal (MGé) and medial (MGm) divisions of the medial genicu- lace complex, with a minor contribution from MGv. ‘The belt region has been subdivided into several different fields on the basis of separate cochlear representations, histo- chemical features, and trends in connectivity patterns. Acknowledging differences in gerrymandering among dif- ferent authors and a paucity of systema studies, we interpret existing data as evidence that the belt area contains seven fields, named according to their relative positions along the superior surface of the superior eempo: ral gyrus (STG; Figures 1 and 2). Cochleotopy has been reported in anterolateral (AL), caudolateral (CL), eaudome- dial (CM), and middle lateral (ML) fields (7,9",10,11 First spike latencies have been found to be longer in the lateral belt chan the core in ¢wo of three studies in alert ‘macaques [23-25]. Puse tone sensitivity in CM relies on the ic microelectrode integrity of AI in anesthetized macaques [11**]. ‘Thus, the belt area represents a second stage in the hierarchical pro cessing of auditory information along the MGy—core—>belt pathway: The belt also processes MGd and MGm inputs in. parallel with core inputs across its several subdivisions. In humans, the distribution of EP response latencies are con sistent with serial processing extending from the core area in TG into surrounding areas along the STG [19,2627] Subdural recordings have identified a cochleotopically organized area on STG lying caudal to TG [28], and pre- liminary functional imaging data suggest two cochleotopic fields on the superior surface of STG [17] that may repre: sent the human homologs of lateral bele fields. Phe parabelt area lies adjacent to the lateral belt fields along. the lateral surface of the STG. The parabelt hi nections with the belt area the core area 12"). Like the helt, the parabele receives thal- amie input from MGd and MGm; in addition, the parabele has strong connections with the medial pulvinar, supra- geniculate, and limitans nuclei [13*]. The rostral parabelt receives inputs selectively from rostral belt fields, whereas the cauclal parabelt receives most inputs from the caudal belt fields. Thus, the parabele lies within a third stage of cor- tical processing within the MGv-score—sbelt—sparabele pathway, ‘The parabele also processes thalamic inputs in par- allel with bele inputs across its subdivisions. In the costral parabelt, neurons are generally sensitive to white noise but not to pure cones [9*]. In the caudal parabelt, most neurons. respond to sounds in contralaceral space, many respond to pure tones over a wide range of frequencies, some manifest motion sensitivity and disection selectivity, and few, if any, are heteromodal, visual, or [29.30]. In macaques, Cebus monkeys, and humans, bilateral lesions that involve the belt and parabele bur spare at least part of the core typically impair auditory pattern perception ‘and minimal connections with somesthetic188 Cognitive neuroscience Now aS) Par Thalamus Gi Miran ce icp 8c Caro Open Nebo ‘Connections and levels of processing in the primate auditory cortex ‘Sold lines denote major connections, and dashed lines denote minor Connections. The main steam of processing invaWves the central ‘nucleus ofthe inferior coliculus (ICc), the ventral nucleus ofthe media {geniculato compiox (Mv), and the core areas ofthe auditory cortex [A parallel stream aso involves the dorsal (Cd) and percental(IGp) divisions ofthe inferior colficulus the dorsal (MGd) and medial (MG) divisions ofthe medial geniculate complex, and the belt cortex. The superior coliculus (SC) projects to parts of the medial pulvinar (PM), suprageniculate (Sp) and limitans (Lim) nucle, as @ possible third source of auditory input tothe parabelt cortex. Additional evels of processing invoive cortex ofthe superior tomporal gyrus (STG) Adjaning the belt and parabel rogions, superior temporal ‘sulcus (STS), and preftntal cortox. The prforental connections of rostral (R} and caudal (C) sectors of cortex are indicated (c.g, discrimination of tone sequences) with little or no effect on sound detection [31-34]. Some human functional imaging studies demonstrate greater STG activation during passive stimulation with speech or music than with noise [35,36]. Auditory priming in humans can be sustained after complete bilateral lesions of the core area, presumably because spared portions of the belt and parabelt continue to receive auditory input via parallel pathways ascending from. nonMGv thalamus [21] and to sustain reciprocal connec tions with memory-related structures Auditory processing extends beyond auditory cortex via connections of the parabelt and, to a lesser extent, the bele with specific regions of adjacent temporal cortex, medial temporal cortex, prefrontal cortex, and parietal cortex, [8,12%,377,38*]. In awake macaques, neuronal activity in auditory cortex is influenced by level of arousal, general attention, directed auditory attention, and perceptual task requirements [25,29,39,40], probably through descending projections from these cortical regions as well as ascending projections from the reticular activating system and no: specific thalamic inputs [41]. Many neurons in these regions are heteromodal and participate in cognitive aspects of auditory processing [3042-45]. In humans, EPs have been recorded in the frontoparietal operculum using intracortical [46] and subdural [47] electrodes. Increased blood flow in dorsolateral prefrontal cortex has been reported during phoneme and pitch diserimination [35], possibly in relation to its role in working memory [48]. Cognitive aspects of auditory processing have been of great interest in human EP and functional imaging studies [49-51]. Lesions involving the temporoparietal junction or posterior parietal cortex, especially in the right hemi- sphere, are often associated with impaired spatial localization, extinction, or frank neglect of auditory stimuli presented in contralateral acoustic space [52]. Similarly, ablations of the inferior parietal lobule and temporoparietal junction in macaques produce hemi-inattention t0 co tralatecal auditory and other sensory stimuli [53]. Right frontal lobe lesions in humans are also associated with auditory hemi-inatcention [54]. Neural coding of spectral, temporal, and spatial information Individual neurons in the core and belt areas change the rate and timing of their activity as a funetion of the spectral ‘content of an auditory stimulus, its temporal features, and its spatial location, Recent quantitative analyses of fre- y-dependent changes in firing rate at threshold and suprathreshold intensities have demonstrated sharp tuning, in alert [55*,56-S8] and anesthetized monkeys [9**,11°*,59]. Populations of Al neurons sensitive to a par- ticular frequency range synchronize their firing during pure tone stimulation, and coordination of spike timing. provides information about che stimulus even when mean firing rates do not change [60]. In anesthetized monkeys, peaks in isointensity and isorate functions for on-excitation are generally sharper in core than in belt areas [9*%1 Whereas neurons in the core region tend w dischasge at higher rates during stimulation with pure tones than with narrowband noise, the opposite is tue of neurons in the lateral belt areas [10]. These results suggest a convergence ‘of inputs from core neurons sensitive to adjacent frequen- cies onto each lateral bele neuron. In general, lateral belt neurons also fire more vigorously during stimulation with species-specific vocalizations chan with pure tones [10]. In the absence of barbiturate anesthesia, many neurons show frequency-dependent pattems of excitation and inh bition that unfold over time in relation to the stimulus — for example, on-excitation at one spectral location, and on- inhibition or off-excitation at another (39,55°,58,61-63]. Receptive field dynamics in auditory cortex may provide a‘Auditory processing in primate cerebral cortex Kaas, Hackett and Tramo 167 neural mechanism for the integration of spectral inforn tion over time necessary to perceive natural sounds, including vocal communication sounds [64]. Recent accounts of developmental and acquired language disorders have emphasized the contribution of temporal processing mechanisms to speech processing in humans [65,66]. Most neurons in unanesthetized squirrel monkey auditory cortex synchronize their firing andfor increase their firing as a function of periodic fluctuations in the temporal lope of complex waveforms [67]. AI neurons general ly show better cemporal resolution than neurons in surrounding areas. Phase-locking to slow envelope Muctu- ations in a species-specific voealization has been observed across subpopulations of AI neurons in barbicurate-anes- thetized marmosets [68]. Averaged multi-unit activiey in AL of unanesthetized macaques is time-locked to abrupt envelope changes in consonant-vowel syllables and to envelope periodicities embedded in vowel sounds and lick trains [69,70,71"]. While there is EP evidence that periodicity pitch is represented by the place of maximal activity in human AI (72), single-unit and averaged multi- unit recordings in_ macaques show no evidence of place-rate coding [73,74]. Because stimulus fundamental frequencies associated with the upper limics of phase-lock- ing and periodicicy-dependent rare changes are well below those associated with pitch percepts for the vast majority of Al neurons, the role of these temporal coding mechanisms in virtual pitch perception has been called into question. In alert human auditory cortex, the excitatory band- widths of isointensity functions for most single neurons recorded by Howard ef af, [18] were roughly compatible with che grain of neuronal frequeney selectivity recorded in alere and anesthetized macaques. The coarsening of Frequency resolution observed in humans after bilateral lesions of core and belt areas [21,57] may be attributable to loss of frequency-selective neurons. Frequency-spe~ shortening of cific narrowing of isorate functions, response latencies, and expansion of areal repre: have been observed in anesthetized ow! monkey AI fol- lowing several weeks of training on a frequency discrimination eask [59]. These results indieate that new: ronal frequency sensitivity and selectivity are dependent on experience into adulthood. In musicians, experience- dependent enlargement of the N100m EP elicited by piano tones relative to pure cones has been reported [7 und the size of the lefe caudal STG surface correlates with early training and absolute pitch ability [76} Neurons in auditory cortex encode spatial location principal- ly through mechanisms of binaural integration that utilize both rate- and time-based codes. Frequeney-selecti rons in the core and lateral belt of awake macaques change their firing rate as a function of interaural intensity differ- ences in the range of approximately 5-25 dB SPL (sound pressure level) and, for tones below about 2 kHz, interaural time delays as low as a few hundred milliseconds (77). Approximately 90% of neurons fire most strongly when a tone or broadband noise is presented at the midline or in the contralateral hemifield [40,78], and there is limited evi- dence suggesting that neurons lying along a given penetration prefer the same spatial location [40]. Many neurons in the core, lateral belt, caudal belt, and caudal parabele manifest broad spatial cuning [29,40]. Spatial selectivity for horizontal separations finer than 10 degrees {about three times the psychophysical thresholds in macaques) has not yet been demonstrated in individual neurons [56], but could be supported by rate information carried by populations of neurons [79]. About one-third of neurons in the core area are sensitive to the presence and direction of motion along the horizontal azimuth; in genet- al, azimuthal location determines the temporal pattern of excitation (e.g, transient on-excitation, sustained ons tation, or off-excitation), magnitude of excitation within the corresponding time epoch [78]. Most prefroncal and posterior parietal neurons respond more strongly or exclusively during processing of contralateral auditory stimuli [44.45] and motion determines the In both humans and macaques, unilateral lesions of supe rior temporal cortex and of connected areas in prefroncal tnd inferior parietal cortex impair the ability co localize ceral_ hemifield 80,81 Inabilicy to detect sound movement using interaural phase and/or amplitude modulation cues has been documented in a patient with a lesion involving the right posterior tem- poral lobe, inferior parietal lobule, and insula [82]. Conclusions Recent studies indicate that the auditory cortex of pri mates has several distinet levels of processing, In the core area, cortical processing is initially carried out in parallel across the thr The three core fields project to a narrow surrounding belt area comprising approximately seven fields, at least four of which exhibit cochleotopie organization. ‘The belt area also 8 secondary e cochleoropically organized fields receives medial geniculate inputs throug pathway. The parabelt atea, a third level of processing, receives inputs from the belt and thalamus and projects co temporal, frontal, and parical cortex for higher stages of processing, The degree to which differences in physiolog- ical response properties and behavioral functions map onto ifferent anatomical stages of processing is an active area of research. In general, results in monkeys and humans are consistent with the notion that spectral and temporal fea tures of sound are extracted in the core area and integrated in the bele and parabele areas to form mental representa tions of auditory objects and their spatial locations. Multimodal integration and cognitive influences on audi- tory percept formation are realized through connections of the parabelt with heteromodal and supramodal cortices Acknowledgements “This work was supported by National nies of Heath arants NS 16446 oJ Tt Ress, DC 002490 TA Hacker, snd DC 3382 wo MY amo168 Cognitive neuroscience References and recommended reading Papers of paricuar interest, published win the annval period of review, have been highighted as + of special intrest sof outstanding interest 1. Glaey 36, Barone Png Physiology of thalamus and cortex. The Mammalian Audlory Pathway: Neurophysiology Ecited by Popper AN, Fay RR. 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