Troy A. Hackett

Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans

The goal of the present study was to determine whether the architectonic criteria used to identify the core region in macaque monkeys (Macaca mulatta, M. nemestrina) could be used to identify a homologous region in chimpanzees (Pan troglodytes) and humans (Homo sapiens). Current models of auditory cortical organization in primates describe a centrally located core region containing two or three subdivisions including the primary auditory area (AI), a surrounding belt of cortex with perhaps seven divisions, and a lateral parabelt region comprised of at least two fields. In monkeys the core region can be identified on the basis of specific anatomical and physiological features. In this study, the core was identified from serial sets of adjacent sections processed for cytoarchitecture, myeloarchitecture, acetylcholinesterase, and cytochrome oxidase. Qualitative and quantitative criteria were used to identify the borders of the core region in individual sections. Serial reconstructions of each brain were made showing the location of the core with respect to gross anatomical landmarks. The position of the core with respect to major sulci and gyri in the superior temporal region varied most in the chimpanzee and human specimens. Although the architectonic appearance of the core areas did vary in certain respects across taxonomic groups, the numerous similarities made it possible to identify unambiguously a homologous cortical region in macaques, chimpanzees, and humans. J. Comp. Neurol. 441:197–222, 2001.

SUBDIVISIONS OF AUDITORY CORTEX AND IPSILATERAL CORTICAL CONNECTIONS OF THE PARABELT AUDITORY CORTEX IN MACAQUE MONKEYS

Auditory cortex of macaque monkeys can be divided into a core of primary or primary‐like areas located on the lower bank of the lateral sulcus, a surrounding narrow belt of associated fields, and a parabelt region just lateral to the belt on the superior temporal gyrus. We determined patterns of ipsilateral cortical connections of the parabelt region by placing injections of four to seven distinguishable tracers in each of five monkeys. Results were related to architectonic subdivisions of auditory cortex in brain sections cut parallel to the surface of artificially flattened cortex (four cases) or cut in the coronal plane (one case). An auditory core was clearly apparent in these sections as a 16‐ to 20‐mm rostrocaudally elongated oval, several millimeters from the lip of the sulcus, that stained darkly for parvalbumin, myelin, and acetylcholinesterase. These features were most pronounced caudally in the cortex assigned to auditory area I, only slightly reduced in the rostral area, and most reduced in the narrower rostral extension we define as the rostrotemporal area. A narrow band of cortex surrounding the core stained more moderately for parvalbumin, acetylcholinesterase, and myelin. Two regions of the caudal belt, the caudomedial area, and the mediolateral area, stained more darkly, especially for parvalbumin. Rostromedial and medial rostrotemporal, regions of the medial belt stained more lightly for parvalbumin than the caudomedial area or the lateral belt. The parabelt region stained less darkly than the core and belt fields. Injections confined to the parabelt region labeled few neurons in the core, but large numbers in parts of the belt, the parabelt, and adjacent portions of the temporal lobe. Injections that encroached on the belt labeled large numbers of neurons in the core and helped define the width of the belt. Caudal injections in the parabelt labeled caudal portions of the belt, rostral injections labeled rostral portions, and both caudal and rostral injections labeled neurons in the rostromedial area of the medial belt. These observations support the concept of dividing the auditory cortex into core, belt, and parabelt; provide evidence for including the rostral area in the core; suggest the existence of as many as seven or eight belt fields; provide evidence for at least two subdivisions of the parabelt; and identify regions of the temporal lobe involved in auditory processing. J. Comp. Neurol. 394:475–495, 1998.

Prefrontal connections of the parabelt auditory cortex in macaque monkeys

In the present study, we determined connections of three newly defined regions of auditory cortex with regions of the frontal lobe, and how two of these regions in the frontal lobe interconnect and connect to other portions of frontal cortex and the temporal lobe in macaque monkeys. We conceptualize auditory cortex as including a core of primary areas, a surrounding belt of auditory areas, a lateral parabelt of two divisions, and adjoining regions of temporal cortex with parabelt connections. Injections of several different fluorescent tracers and wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) were placed in caudal (CPB) and rostral (RPB) divisions of the parabelt, and in cortex of the superior temporal gyrus rostral to the parabelt with parabelt connections (STGr). Injections were also placed in two regions of the frontal lobe that were labeled by a parabelt injection in the same case. The results lead to several major conclusions. First, CPB injections label many neurons in dorsal prearcuate cortex in the region of the frontal eye field and neurons in dorsal prefrontal cortex of the principal sulcus, but few or no neurons in orbitofrontal cortex. Fine-grain label in these same regions as a result of a WGA-HRP injection suggests that the connections are reciprocal. Second, RPB injections label overlapping prearcuate and principal sulcus locations, as well as more rostral cortex of the principal sulcus, and several locations in orbitofrontal cortex. Third, STGr injections label locations in orbitofrontal cortex, some of which overlap those of RPB injections, but not prearcuate or principal sulcus locations. Fourth, injections in prearcuate and principal sulcus locations labeled by a CPB injection labeled neurons in CPB and RPB, with little involvement of the auditory belt and no involvement of the core. In addition, the results indicated that the two frontal lobe regions are densely interconnected. They also connect with largely separate regions of the frontal pole and more medial premotor and dorsal prefrontal cortex, but not with the extensive orbitofrontal region which has RPB and STGr connections. The results suggest that both RPB and CPB provide the major auditory connections with the region related to directing eye movements towards stimuli of interest, and the dorsal prefrontal cortex for working memory. Other auditory connections to these regions of the frontal lobe appear to be minor. RPB has connections with orbitofrontal cortex, important in psychosocial and emotional functions, while STGr primarily connects with orbital and polar prefrontal cortex.

Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions.

In this study and its companion, the cortical and subcortical connections of the medial belt region of the marmoset monkey auditory cortex were compared with the core region. The main objective was to document anatomical features that account for functional differences observed between areas. Injections of retrograde and bi‐directional anatomical tracers targeted two core areas (A1 and R), and two medial belt areas (rostromedial [RM] and caudomedial [CM]). Topographically distinct patterns of connections were revealed among subdivisions of the medial geniculate complex (MGC) and multisensory thalamic nuclei, including the suprageniculate (Sg), limitans (Lim), medial pulvinar (PM), and posterior nucleus (Po). The dominant thalamic projection to the CM was the anterior dorsal division (MGad) of the MGC, whereas the posterior dorsal division (MGpd) targeted RM. CM also had substantial input from multisensory nuclei, especially the magnocellular division (MGm) of the MGC. RM had weak multisensory connections. Corticotectal projections of both RM and CM targeted the dorsomedial quadrant of the inferior colliculus, whereas the CM projection also included a pericentral extension around the ventromedial and lateral portion of the central nucleus. Areas A1 and R were characterized by focal topographic connections within the ventral division (MGv) of the MGC, reflecting the tonotopic organization of both core areas. The results indicate that parallel subcortical pathways target the core and medial belt regions and that RM and CM represent functionally distinct areas within the medial belt auditory cortex. J. Comp. Neurol. 496:72–96, 2006.

Subdivisions of auditory cortex and levels of processing in primates

In a series of experiments on New World and Old World monkeys, architectonic features of auditory cortex were related to tone frequency maps and patterns of connections to generate and evaluate theories of cortical organization. The results suggest that cortical processing of auditory information involves a number of functionally distinct fields that can be broadly grouped into four or more levels of processing. At the first level, there are three primary-like areas, each with a discrete pattern of tonotopic organization, koniocortical histological features, and direct inputs from the ventral division of the medial geniculate complex. These three core areas are interconnected and project to a narrow surrounding belt of perhaps seven areas which receive thalamic input from the major divisions of the medial geniculate complex, the suprageniculate/limitans complex, and the medial pulvinar. The belt areas connect with a lateral parabelt region of two or more fields that are almost devoid of direct connections with the core and the ventral division of the medial geniculate complex. The parabelt fields connect with more distant cortex in the superior temporal gyrus, superior temporal sulcus, and prefrontal cortex. The results indicate that auditory processing involves 15 or more cortical areas, each of which is interconnected with a number of other fields, especially adjoining fields of the same level.

Information flow in the auditory cortical network

Auditory processing in the cerebral cortex is comprised of an interconnected network of auditory and auditory-related areas distributed throughout the forebrain. The nexus of auditory activity is located in temporal cortex among several specialized areas, or fields, that receive dense inputs from the medial geniculate complex. These areas are collectively referred to as auditory cortex. Auditory activity is extended beyond auditory cortex via connections with auditory-related areas elsewhere in the cortex. Within this network, information flows between areas to and from countless targets, but in a manner that is characterized by orderly regional, areal and laminar patterns. These patterns reflect some of the structural constraints that passively govern the flow of information at all levels of the network. In addition, the exchange of information within these circuits is dynamically regulated by intrinsic neurochemical properties of projecting neurons and their targets. This article begins with an overview of the principal circuits and how each is related to information flow along major axes of the network. The discussion then turns to a description of neurochemical gradients along these axes, highlighting recent work on glutamate transporters in the thalamocortical projections to auditory cortex. The article concludes with a brief discussion of relevant neurophysiological findings as they relate to structural gradients in the network.

Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing.

Recent findings in both monkeys and humans indicate that multisensory convergence occurs in low-level cortical structures generally believed to be unisensory in function. In an in-depth treatment of this theme, this paper reviews anatomical and physiological findings relating to the convergence of visual, somatosensory and auditory signals at early stages of auditory cortical processing. We discuss the potential anatomical sources of the input, and the types of known projections, and attempt to integrate this information with the current hierarchical model of auditory processing. Finally, we consider the functional implications of multisensory integration in early sensory processing.

Thalamocortical connections of the parabelt auditory cortex in macaque monkeys

The auditory cortex of macaque monkeys contains a core of primary‐like areas surrounded by a narrow belt of associated fields that encompass much of the superior temporal plane in these animals. Adjacent to the lateral belt on the superior temporal gyrus is a parabelt region that contains at least two subdivisions (rostral and caudal). In a previous study (Hackett et al. [1998] J. Comp. Neurol. 394:475–495), we determined that the parabelt has topographic connections with the belt areas surrounding the core, but minimal connections with the core itself. In this study, we describe the thalamocortical connections of the parabelt auditory cortex based on multiple injections of neuronal tracers into this region in each of five macaque monkeys. Injections confined to the parabelt labeled large numbers of neurons in the dorsal (MGd) and magnocellular (MGm) divisions of the medial geniculate complex (MGC), suprageniculate (Sg), limitans (Lim), and medial pulvinar (PM) nuclei. Only when injections encroached on the lateral belt cortex were substantial numbers of labeled neurons found in the ventral (MGv) division of the MGC, consistent with the absence of significant connections between the parabelt and core fields. The rostrocaudal topography of the parabelt region was maintained in the thalamocortical connections, supporting the parcellation of this region of cortex. The results suggest that the parabelt region represents a third level of auditory cortical processing, which is not influenced by direct inputs from primary cortical or subcortical auditory structures. J. Comp. Neurol. 400:271–286, 1998.

Multisensory convergence in auditory cortex, I. Cortical connections of the caudal superior temporal plane in macaque monkeys

The caudal medial auditory area (CM) has anatomical and physiological features consistent with its role as a first‐stage (or “belt”) auditory association cortex. It is also a site of multisensory convergence, with robust somatosensory and auditory responses. In this study, we investigated the cerebral cortical sources of somatosensory and auditory inputs to CM by injecting retrograde tracers in macaque monkeys. A companion paper describes the thalamic connections of CM (Hackett et al., J. Comp. Neurol. [this issue]). The likely cortical sources of somatosensory input to CM were the adjacent retroinsular cortex (area Ri) and granular insula (Ig). In addition, CM had reliable connections with areas Tpt and TPO, which are sites of multisensory integration. CM also had topographic connections with other auditory areas. As expected, connections with adjacent caudal auditory areas were stronger than connections with rostral areas. Surprisingly, the connections with the core were concentrated along its medial side, suggesting that there may be a medial‐lateral division of function within the core. Additional injections into caudal lateral auditory area (CL) and Tpt showed similar connections with Ri, Ig, and TPO. In contrast to CM injections, these lateral injections had inputs from parietal area 7a and had a preferential connection with the lateral (gyral) part of Tpt. Taken together, the findings indicate that CM may receive somatosensory input from nearby areas along the fundus of the lateral sulcus. The differential connections of CM compared with adjacent areas provide additional evidence for the functional specialization of the individual auditory belt areas. J. Comp. Neurol. 502:894–923, 2007.

Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane.

Recent studies of macaque monkey auditory cortex have revealed convergent auditory and somatosensory activity in the caudomedial area (CM) of the belt region. In the present study and its companion (Smiley et al., J. Comp. Neurol. [this issue]), neuroanatomical tracers were injected into CM and adjacent areas of the superior temporal plane to identify sources of auditory and somatosensory input to this region. Other than CM, target areas included: A1, caudolateral belt (CL), retroinsular (Ri), and temporal parietotemporal (Tpt). Cells labeled by injections of these areas were distributed mainly among the ventral (MGv), posterodorsal (MGpd), anterodorsal (MGad), and magnocellular (MGm) divisions of the medial geniculate complex (MGC) and several nuclei with established multisensory features: posterior (Po), suprageniculate (Sg), limitans (Lim), and medial pulvinar (PM). The principal inputs of CM were MGad, MGv, and MGm, with secondary inputs from multisensory nuclei. The main inputs of CL were Po and MGpd, with secondary inputs from MGad, MGm, and multisensory nuclei. A1 was dominated by inputs from MGv and MGad, with light multisensory inputs. The input profile of Tpt closely resembled that of CL, but with reduced MGC inputs. Injections of Ri also involved CM but strongly favored MGm and multisensory nuclei, with secondary inputs from MGC and the inferior division (VPI) of the ventroposterior complex (VP). The results indicate that the thalamic inputs of areas in the caudal superior temporal plane arise mainly from the same nuclei, but in different proportions. Somatosensory inputs may reach CM and CL through MGm or the multisensory nuclei but not VP. J. Comp. Neurol. 502:924–952, 2007.