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Keywords:

  • primate;
  • auditory cortex;
  • thalamus;
  • medial geniculate;
  • medial pulvinar

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED

The primate auditory cortex is comprised of a core region of three primary areas, surrounded by a belt region of secondary areas and a parabelt region lateral to the belt. The main sources of thalamocortical inputs to the auditory cortex are the medial geniculate complex (MGC), medial pulvinar (PM), and several adjoining nuclei in the posterior thalamus. The distribution of inputs varies topographically by cortical area and thalamic nucleus, but in a manner that has not been fully characterized in primates. In this study, the thalamocortical connections of the lateral belt and parabelt were determined by placing retrograde tracer injections into various areas of these regions in the marmoset monkey. Both regions received projections from the medial (MGm) and posterodorsal (MGpd) divisions of the medial geniculate complex (MGC); however, labeled cells in the anterodorsal (MGad) division were present only from injections into the caudal belt. Thalamic inputs to the lateral belt appeared to come mainly from the MGC, whereas the parabelt also received a strong projection from the PM, consistent with its position as a later stage of auditory cortical processing. The results of this study also indicate that the organization of the marmoset auditory cortex is similar to other primates. Anat Rec, 2012. © 2012 Wiley Periodicals, Inc.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED

This working model of auditory cortex is based on studies of both New and Old World monkeys (for reviews see: Pandya, 1995; Kaas and Hackett, 1998, 2000; Rauschecker, 1998; Kaas et al., 1999; Hackett, 2002, 2011; Jones, 2003) (Fig. 1). A main component of this model is that auditory cortex includes areas of cortex that receive preferential input from the medial geniculate complex (MGC) (Fig. 1). Based on this definition, three regions of the superior temporal cortex are identified as part of auditory cortex in primates: core, belt, and parabelt. The core region, receives input mainly from the ventral division of the medial geniculate complex (MGv) (Burton and Jones, 1976; Jones and Burton, 1976; Fitzpatrick and Imig, 1978; Luethke et al., 1989; Morel and Kaas, 1992; Morel et al., 1993; Pandya et al., 1994; Hashikawa et al., 1995; Molinari et al., 1995; de la Mothe et al., 2006b) and consists of three areas [auditory area 1 (A1), rostral area (R), and rostrotemporal area (RT)]. It is surrounded both medially and laterally by a belt region of eight areas [caudomedial (CM), middle medial (MM), rostromedial (RM), rostrotemporal medial (RTM), caudolateral (CL), middle lateral (ML), anterolateral (AL), and rostrotemporal lateral (RTL)] that receives input preferentially from the dorsal division of the medial geniculate complex (MGd) (Burton and Jones, 1976; Morel and Kaas, 1992; Pandya et al., 1994; Molinari et al., 1995; Rauschecker et al., 1997; de la Mothe et al., 2006b). The parabelt region, located lateral to the belt, is divided into two areas [caudal parabelt (CPB) and rostral parabelt (RPB)] and also receives input from MGd (Hackett et al., 1998b). Additional areas that are responsive to auditory stimuli (temporal, prefrontal, and posterior parietal cortex), but do not have principal inputs from the MGC are referred to as auditory-related fields (Hackett, 2011).

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Figure 1. Schematic model of the marmoset auditory cortex and medial geniculate complex. The lateral sulcus (LS) of the left hemisphere was graphically opened (cut) to reveal the locations of auditory cortical areas otherwise hidden. The three regions of auditory cortex are identified with varying degrees of shading: core (dark shading), belt (light shading), and parabelt (medium shading). The four divisions of the MGC are identified with varying degrees of shading: MGv (dark shading), dorsal divisions MGad (medium shading), MGpd (light shading), and MGm (no shading). Based on the primate model of auditory cortex, black lines denote proposed projections from dorsal divisions in the MGC to areas in the belt and parabelt regions. Additional nuclei identified include: suprageniculate (Sg), posterior nucleus (Po), limitans (Lim), medial pulvinar (PM), lateral pulvinar (PL), inferior pulvinar (PI), and lateral geniculate nucleus (LGN). ITG, inferior temporal gyrus; LS, lateral sulcus; PV, parietoventral area; Pro, proisocortical area; Ri, retroinsular area; S2, somatosensory area 2; STGr, rostral superior temporal gyrus; STS, superior temporal sulcus; Tpt, temporal parietotemporal area; D, dorsal; L, lateral; M, medial; R, rostral.

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Information in auditory cortex is thought to be processed both serially and in parallel (Rauschecker et al., 1997; Hackett et al., 1998a, b; Kaas and Hackett, 1998; Rauschecker, 1998; Kaas et al., 1999; Hackett and Kaas, 2003; Hackett, 2011). Serial organization is based in part on connectional studies, including the companion to this study, where the core projects to the belt, but not the parabelt; implying that the belt areas are the principal source of auditory cortical inputs to the parabelt (Morel and Kaas, 1992; Morel et al., 1993; Hackett et al., 1998a; de la Mothe et al., 2012). Thus, the belt and parabelt regions exhibit distinct cortical connection patterns in that the belt is strongly connected with both the core and the parabelt,while the parabelt is strongly connected with the belt. The processing hierarchy established by the cortical connections is also reflected in the organization of thalamic inputs to these regions.

The most well-established feature is that the core areas receive their main thalamic input from MGv (Burton and Jones, 1976; Fitzpatrick and Imig, 1978; Luethke et al., 1989; Morel and Kaas, 1992; Morel et al., 1993; Pandya et al., 1994; Molinari et al., 1995; de la Mothe et al., 2006b), while both the belt and parabelt lack these strong MGv projections and receive their main inputs from MGd (Burton and Jones, 1976; Morel and Kaas, 1992; Molinari et al., 1995; Hackett et al., 1998b, 2007a, b). Even though both regions receive a major input from MGd, one distinguishing characteristic of the parabelt region is the strong input from the medial pulvinar (PM). PM differs from other multisensory nuclei that project to auditory cortex [suprageniculate (Sg), limitans (Lim), posterior nucleus (Po)] in that it has connections with higher order areas such as prefrontal and limbic cortex (Romanski et al., 1997). The strong PM projection to the parabelt but not the belt is consistent with the notion that the parabelt is a later stage of processing in auditory cortex.

A second feature of organization is that the thalamic connections of auditory cortex are topographic. Injections into lateral belt and parabelt regions, for example, have revealed topographic connection patterns with cortical areas (Morel and Kass, 1992; Hackett et al., 1998a; Romanski et al., 1999) as well as with MGd (Burton and Jones, 1976; Morel and Kaas, 1992; Pandya et al., 1994; Molinari et al., 1995; Hackett et al., 1998b; de la Mothe et al., 2006b), which is commonly subdivided into anterior and posterior divisions (MGad and MGpd) (Fig. 1). Molinari et al. (1995) reported that projections from MGad and MGpd were concentrated in the caudal and rostral areas of the lateral belt, respectively, in macaque monkeys. Hackett et al. (2007a, b) also reported preferential connections of the caudal belt areas (CM and CL) with MGad. This is consistent with results from our previous studies of the medial belt region in marmosets where MGad was preferentially connected with CM and MGpd with RM (de la Mothe et al., 2006b). Based on these findings, it is reasonable to predict that rostral and caudal areas of the lateral belt and parabelt in the marmoset would reveal similar topographic patterns.

One goal of this study and its companion (de la Mothe et al., 2012) was to expand our understanding of the organization of the marmoset auditory cortex by examining the cortical and thalamic connections of the lateral belt and parabelt regions, complementing the thalamocortical projections of the core and medial belt revealed from previous studies in the same cases (de la Mothe et al., 2006a, b). A second goal of this study was to test the following tenets of our working model of primate auditory cortex organization: (1) the lateral belt and the parabelt regions have distinct patterns of thalamic input reflective of their hierarchical position that include a lack of MGv projections and differences in the projections from PM and (2) the lateral belt and parabelt regions have topographic patterns of thalamic input. In combination with results from our previous medial belt and core studies, results of this study suggests that the fundamental organization of the marmoset is consistent with the basic principles of the primate model of auditory cortex and that these principles are highly conserved in New World and Old World monkeys, including the marmoset, owl monkey (Fitzpatrick and Imig, 1978, 1980; Imig et al., 1977; Morel and Kaas, 1992) and macaque monkey.

MATERIALS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED

The experiments proposed in this report were conducted in accordance with the Vanderbilt University Institutional Animal Care and Use Committee Guidelines and the Animal Welfare Act under a protocol approved by the Vanderbilt University Institutional Animal Care and Use Committee. Four adult marmosets (Callithrix jacchus jacchus) served as animal subjects in this study. The experimental history of each animal is included in Table 1. Because the current articles on the lateral belt and parabelt are extensions of the previous medial belt and core studies, descriptions of these experimental procedures have been reported elsewhere (de la Mothe et al., 2006b) but are described briefly here.

Table 1. Experimental history of animal subjects
Case no.CaseSexAreas injectedTracer%Volume (μL)
  1. Areas of tracer injections (CL, caudolateral belt; ML, mediolateral belt; AL, anterolateral belt; CPB, caudal parabelt; RPB, rostral parabelt). Neuroanatomical tracers (CTB-red, cholera toxin subunit B 594; FR, fluororuby; DY; diamidino yellow), aqueous concentration, and volume injected are listed for each tracer.

1(01–89)MCL/CMFR100.30
CPBDY100.30
2(03–59)MCPBCTB-red10.35
3(04–40)MRPBCTB-red10.35
4(04–51)MALFR100.30

General Surgical Procedures

Pressure injections of anatomical tracers were made into subdivisions of auditory cortex in marmoset monkeys under aseptic conditions. Anesthesia was maintained by a ketamine hydrochloride (10 mg/kg)/xylazine (0.4 mg/kg) combination or 2%–3% isoflurane. Anesthesia levels were adjusted based on vital signs (body temperature, heart rate, expiratory CO2, and O2 saturation) which were continuously monitored throughout the surgery. The head was stabilized with a stereotaxic instrument (David Kopf Instruments, Tujunga, CA) and a midline incision was made exposing the skull, followed by retraction of the left temporal muscle. A craniotomy exposing the superior temporal gyrus and the lateral sulcus was made, after which the dura was cut and retracted. Following the injections, the exposed area of the brain was covered with softened gelfilm, the craniotomy closed with dental acrylic, and the overlying temporal muscle and skin was sutured back into place.

Injections and Perfusion

Injections of tracers were made into target areas using 1- to 2-μL syringes, with a pulled glass pipette tip, attached to a hydraulic microdrive. Injections were made into the lateral belt and parabelt regions by using landmarks and blood vessels, on the lateral surface of the superior temporal gyrus (STG), to locate auditory cortex. The injections were made directly into the auditory areas. In all cases, the injections made were manual pressure injections of various amounts (Table 1) after which the syringe remained for approximately 10 minutes under continuous observation to maximize uptake and minimize leakage. The tracers used were Alexa Fluor 594 conjugated cholera toxin-B (CTB-red) (Invitrogen Corp.); fluororuby (FR); and diamidino yellow (DY). Because of the various levels of sensitivity of the tracers the amounts and solution concentrations were varied accordingly as shown in the table.

At the end of the experiment (between 10 and 14 days after injections), a lethal dose of pentobarbital was administered. Just before cardiac arrest, the animal was perfused through the heart with warm saline followed by cold 4% paraformaldehyde dissolved in 0.1 M phosphate buffer. Immediately following the perfusion, the brains were removed, the two hemispheres and the brainstem were separated, placed in 30% sucrose for several days, and then blocked.

Histology and Data Analysis

The thalamus was cut perpendicular to long axis of the brainstem at 40 μm. Depending on the case, series of sections were processed for the following: (i) fluorescent microscopy; (ii) CTB; (iii) myelin (Gallyas, 1979); (iv) acetylcholinesterase (AChE) (Geneser-Jensen and Blackstad, 1971); (v) stained for Nissl substance with thionin; (vi) cytochrome oxidase (CO) (Wong-Riley, 1979); or (vii) parvalbumin immunohistochemistry (Pv).

Cells labeled with fluorescent tracers were all plotted on an XY plotter (Neurolucida) coupled to a Leitz microscope under ultraviolet illumination. Drawings of each section were made, noting architectonic boundaries, the location of blood vessels and the distribution of labeled cells. Architecture of the marmoset thalamus was established in our previous studies (de la Mothe et al., 2006b) and provided the criteria for identifying the borders (Fig. 2). To summarize, borders for MGv were defined by the smallest cells, densest expression of CO, and lamellar arrangement of fibers. Although MGad had similar cell spacing to MGv and greater cell density than the MGpd, expression of CO decreased slightly from MGv, though still more densely expressed than in MGpd which exhibited moderate expression of CO. MGpd also had dense expression of AChE and medium-sized cells of uniform spacing. Cells were most heterogeneous in MGm where the largest cells occupied the ventral two thirds and smaller cells inhabited the dorsal third coextensive with dense AChE expression. Expression of CO in the MGm was patchy throughout, but was most dense in the ventral portion. Fiber density in the medial division was the highest where the brachium of the inferior colliculus (BrIC) passes through the lateral MGC. Injection sites were identified and compared with cortical borders using previously established cortical criteria (de la Mothe et al., 2006a) described in the companion paper to verify location of injections (Fig. 3). These cortical criteria included a core region of dense fibers, AChE, and CO expression; a belt that decreased in CO and AChE expression in the middle layers; and a parabelt that had a weakening of myelination in the infragranular layers.

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Figure 2. Architecture of the marmoset medial geniculate complex. Images of corresponding sections of (A) nissl, (B) CO, and (C) myelin with borders drawn to identify the various divisions based on respective architectonic criteria. Scale bar = 500 μm. D, dorsal; L, lateral.

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Figure 3. Example of an injection site and corresponding reconstructions of architectonic borders. (A) CTB-red injection into CPB, (B) AChE, (C) myelin, and (D) nissl with borders drawn to identify the various areas. Scale bar = 250 μm. D, dorsal; L, lateral.

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A composite drawing was made from adjacent sections processed for label, AChE, myelin, CO, and Nissl by aligning common architectonic borders and blood vessels. Reconstructions of the composite images were achieved using Canvas 8.0 software (Deneba software, Miami, FL) and were analyzed to reveal the individual connection patterns as well as the patterns of injections at similar or dissimilar locations. Cell counts were performed and converted to percentages to better compare the general connection patterns between tracers due to possible variability in tracer sensitivity.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED

Thalamic Connections of the Lateral Belt

In case 1 (Fig. 4), an injection of FR was made into the caudal belt just posterior to A1 that involved both CM and CL. In the most caudal sections, there was sparse retrograde label in the posterodorsal, anterodorsal, and ventral divisions of the MGC (section no. 208-214). In general, the number of labeled cells increased rostrally with the strongest projections from MGad and MGm (section no. 220-232). In the most rostral sections, as the size of the MGC decreased the majority of label was focused in MGad (section no. 238-244). Only sparse label was present throughout MGv. Connections were also present with MGpd, but were weaker relative to MGad. Overall, the connections were focused more in the anterior portion of the MGC with the strongest connections from MGad and MGm. There were some sparse labeled cells in Sg as well as rostrally with VP and PI.

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Figure 4. Thalamic connections of CM/CL and CPB, case 1. Series of reconstructed serial sections are arranged from rostral (upper left) to caudal (lower right). FR-labeled cells (red-filled triangles) and DY-labeled cells (black-filled circles) are drawn onto each section, showing borders between areas identified by architectonic criteria. (Inset) Schematic of marmoset auditory cortex showing location of FR injection in CM/CL and DY injections into caudal CPB. D, dorsal; L, lateral.

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In case 4 (Fig. 5), a FR injection was made into the rostral belt area RTL. In the most caudal section, there was strong label in MGpd, MGm, as well as connections with MGv (possibly due to encroachment of the RT border) (section no. 340). These connections decreased rostrally, though remained present in these subdivisions (section no. 346-364) and included sparse cells in Sg. Caudally, there were weak connection with BIC and PPN (section no. 340-352). In the most rostral sections, sparse label was present in MGad, MGv, MGm, Po, Lim, PM, and CM (section no. 370-384). The majority of the label from this injection was concentrated in the posterior portion of the MGC. Label in MGm was concentrated in the ventral third of the division.

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Figure 5. Thalamic connections of RTL, case 4. Series of reconstructed serial sections are arranged from rostral (upper left) to caudal (lower right). FR-labeled cells (filled triangles) are drawn onto each section, showing borders between areas identified by architectonic criteria. (Inset) Schematic of marmoset auditory cortex showing location of FR injection in rostral RTL. D, dorsal; L, lateral.

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Summary of Thalamic Connections of the Lateral Belt

Injections into both caudal and rostral portions of the lateral belt revealed connections that were confined mainly to the MGC of the thalamus (Fig. 6). Both areas had strong connections with MGm but differed in the relative location of these projections within the division. Label from the caudal belt injection was concentrated in the dorsal half of MGm while labeled cells from the injection into RTL favored the ventral portion. An additional difference between caudal and rostral lateral belt injections was with regard to connections of MGad and MGpd. The CM/CL injection revealed a preferential connection with MGad while RTL was preferentially connected with MGpd.

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Figure 6. Summary of thalamic connections of CM/CL and RTL. Top panels illustrate subcortical connections (arrows) of CM/CL and RTL on schematic diagrams of marmoset auditory cortex and thalamus. Arrow and line size is proportional to connection strength, as indicated in the histograms below each panel. Lines were not drawn for connections representing less than 5% of total. D, dorsal; L, lateral; M, medial; R, rostral.

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Thalamic Connections of the Parabelt

In case 1 (Fig. 4), the DY injection was made into the caudal portion of CPB. In the most caudal sections, label was confined predominantly to the dorsal portion of MGm, which coincided with an AChE dense region, with sparse label also present in MGpd and Sg (section no. 208-214). Moving rostrally, this AChE dense region of MGm was displaced by the Sg which coincides with label shifted to mainly Sg and sparse label remaining in MGm and MGpd (section no. 220-226). Label continued to shift dorsally in the section to occupy Po, Lim, and PM (section no. 232-228), and in the most rostral sections, label was present exclusively in PM (section no. 244).

In case 2 (Fig. 7), an injection of CTB-red was made into the rostral portion of CPB. There were strong connections caudally with MGpd and MGm as well as weak connections with PPN (section no. 117-105). Labeled cells in MGm and MGpd were confined to the dorsal portions of those divisions, similar to the pattern of MGm in case 1, described earlier. More rostrally, labeled cells transitioned from MGC to mainly Sg (section no. 99-93) and this dorsal shift continued with labeled cells occupying Po and Lim in the more anterior sections (section no. 87-75). In the most rostral sections, strong connections were exclusive within PM and labeled cells were focused medially along the MD border and toward the dorsal edge of the section (section no. 69-51). While the majority of the projections from MGC favored the more posterior portion, overall the strongest connections were anterior with the multisensory nuclei Sg, Po, Lim, and PM.

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Figure 7. Thalamic connections of CPB, case 2. Series of reconstructed serial sections are arranged from rostral (upper left) to caudal (lower right). CTB-red-labeled cells (filled triangles) are drawn onto each section, showing borders between areas identified by architectonic criteria. (Inset) Schematic of marmoset auditory cortex showing location of CTB-red injection in rostral CPB. D, dorsal; L, lateral.

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In case 3 (Fig. 8), an injection of FR was made into the rostral portion of RPB. In the most caudal sections, label was distributed predominantly throughout the divisions of MGm and MGpd (section no. 316-322). Label remained in these divisions and expanded to include Sg and some weaker connections with MGad and MGv (section no. 328). There was a decrease in overall labeling in the next rostral section which included a few cells in Lim, Sg, MGpd, MGm, and MGv (section no. 334). Continuing rostrally, connections strengthened and were present mainly in MGm, Lim, and PM with sparse label in Po and PPN (section no. 340). In the rostral sections, while there was sparse label in PPN, Lim, MD, and CM, the majority of the label was confined to the medial portion of PM (section no. 346-364).

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Figure 8. Thalamic connections of RPB, case 3. Series of reconstructed serial sections are arranged from rostral (upper left) to caudal (lower right). CTB-red-labeled cells (filled triangles) are drawn onto each section, showing borders between areas identified by architectonic criteria. (Inset) Schematic of marmoset auditory cortex showing location of CTB-red injection in RPB. D, dorsal; L, lateral.

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Summary of Thalamic Connections of the Parabelt

Injections into the parabelt revealed strong connections with MGm from both rostral and caudal areas, however, caudal injections tended to have projections confined to the dorsal portion of MGm (coinciding with a dense AChE region), while the rostral injection revealed label distributed throughout MGm (Fig. 9). Differences were also apparent from connections with MGpd which was strongly connected to RPB and moderately connected to CPB. Connections between MGpd and the parabelt decreased from rostral to caudal overall with weaker projections from caudal CPB relative to rostral CPB. Outside the MGC, there were strong connections to CPB from Sg, Lim, Po, and PM with the inputs from PM accounting for the largest percentage (35%). RPB also had strong connections with PM and was moderately connected with Sg and Lim. It appears that rostral and caudal connections of the parabelt involve mainly the same nuclei, but the topographic relationships are distinct. Most notably, inputs from the MGpd increase with rostral location in the parabelt, whereas inputs from the multisensory nuclei increase caudally.

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Figure 9. Summary of thalamic connections of CPB and RPB. Top panels illustrate subcortical connections (arrows) of CPB and RPB on schematic diagrams of marmoset auditory cortex and thalamus. Arrow and line size is proportional to connection strength, as indicated in the histograms below each panel. Lines were not drawn for connections representing less than 5% of total. D, dorsal; L, lateral; M, medial; R, rostral.

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DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED

In this study, injections were made into rostral and caudal areas of the lateral belt (CM/CL, RTL) and the parabelt (CPB, RPB) regions of the marmoset auditory cortex. Examination of the labeling patterns between regions revealed topographic thalamocortical connections specific to the belt and the parabelt, and despite the low number of injections into various areas, the results within regions were in general consistent with the literature. The lateral belt was almost exclusively connected with the MGC, while the parabelt had strong connections both within and outside of the MGC, in particular with PM. Within each region, rostral and caudal areas exhibited distinct patterns of connections with these nuclei. The results of this study are consistent with previous studies in other primates and support the predictions of the working model of the primate auditory cortex. In addition, this work, together with our previous studies in the same animals of the core and medial belt regions (de la Mothe et al., 2006a, b), extends our understanding of the anatomical organization of the marmoset monkey (Fig. 10). The significance of these results is discussed below.

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Figure 10. Summary of major regional thalamocortical connection patterns of the marmoset auditory cortex. Divisions of the MGC are illustrated as squares with various shading. Thin black lines, thick black lines, large bold dashed lines, and small dashed lines denote connections from the dorsal divisions of the MGC, the MGm, the MGv, and the medial pulvinar (PM), respectively. Regions reported in the current study are outlined with a thick black line.

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Regional Comparison of the Lateral Belt and the Parabelt

In this study, the lateral belt and parabelt regions received strong input from MGm, consistent with results in macaque and owl monkeys showing that MGm projects to all areas of auditory cortex (Burton and Jones, 1976; Morel and Kaas, 1992; Morel et al., 1993; Hashikawa et al., 1995; Molinari et al., 1995). Apart from strong MGm input, the patterns of the two regions vary in two significant ways. First, input to the lateral belt appears to be confined mainly to the MGC, primarily the two dorsal divisions (MGad, MGpd), whereas the parabelt region, also receives a strong projection from PM with additional inputs from MGpd, Sg, Lim, and Po. Second, while previous work in the macaque parabelt revealed that MGad projected to CPB and the MGpd to RPB (Hackett et al., 1998b), this study of marmoset parabelt did not reveal input from MGad to CPB from either injection. Additional studies, especially those that involved injections into MGad, would be helpful in resolving this discrepancy.

Consistent with previous studies in macaques, however, is that, the parabelt also receives a strong input from PM (Hackett et al., 1998b; Kosmal et al., 1997), a multisensory nucleus in the thalamus with projections to higher order areas (prefrontal, limbic cortex) (Romanski et al., 1997). The concentration of cells in PM was mainly in the medial portion, which has been associated with auditory cortex (Trojanowski and Jacobson, 1975, 1976; Romanski et al., 1997; Hackett et al., 1998b). The strong connections between PM and the parabelt are consistent with the position of the parabelt as a later stage in the hierarchy of auditory cortex (Hackett, 2011) as often claimed for higher order areas which receive strong pulvinar inputs (DeVito and Simmons, 1976; Markowitsch et al., 1985; Yeterian and Pandya, 1989; Schmamann and Pandya, 1990; Cusick et al., 1993). The strong links between the pulvinar and parabelt may also indicate that the parabelt is involved in the proposed corticothalamocortical (CTC) circuits that serve to relay information between cortical areas (Sherman and Guillery, 2001; Guillery and Sherman, 2002; Sherman and Guillery, 2002; Sherman, 2007). If so, such connections could provide an additional means by which auditory and non-auditory information is integrated in cortex.

Topographic Distribution of Thalamic Inputs to the Lateral Belt and the Parabelt

In previous studies of the auditory thalamocortical system in primates, a general observation has been that rostral areas of auditory cortex tend to receive input from the posterior portion of the MGC and caudal areas receive input from anterior MGC (Burton and Jones, 1976; Luethke et al., 1989; Morel and Kaas, 1992; Pandya et al., 1994; Molinari et al., 1995; Hackett et al., 1998b; de la Mothe et al., 2006b). In this study, clear topographic patterns were observed in the thalamocortical projections to the lateral belt and parabelt. In the lateral belt, the MGad projected to the caudal belt areas (CM, CL) and MGpd projected to RTL. This is consistent with previous studies of these areas in macaques (Molinari et al., 1995; Hackett et al., 2007a). Molinari et al. (1995) placed injections in both rostral and caudal areas of the lateral belt in macaque. The rostral belt injection labeled cells in MGpd and MGm, and the caudal lateral belt injection labeled cells in MGad and MGpd. An additional caudal belt injection that was more caudal and medial labeled cells mainly in MGad. Topography along the rostrocaudal axis has also been found in the medial belt. In our previous studies of these areas, injections into the rostral medial belt area, RM, revealed connections with MGpd, while injections into the caudal medial belt areas, MM and CM, revealed preferential connections with MGad (de la Mothe et al., 2006b). While injections into both MM and CM revealed principal inputs from MGad, the more caudal area, CM, also had connections that were more distributed in multisensory nuclei. The caudal belt injection in the present study, which involved CM and CL, had connections concentrated in MGad, but connections with the multisensory nuclei were not as broadly distributed among the multisensory nuclei as was reported in CM. The differences between the lateral and medial belt areas are in some ways consistent with the root-core-belt model proposed by Galaburda and Pandya (1983) in which the root (medial belt) fields were identified as a separate line/region from the belt (lateral belt) fields. A preference for multisensory thalamic projections to the medial belt region has been reported in previous studies (Burton and Jones, 1976; Pandya et al., 1994) and the root areas have been proposed to have role in multimodal processing (Pandya et al., 1994). Other studies have reported multisensory input to the caudal belt that involved area CL (Hackett et al., 2007a; Cappe et al., 2009), in contrast to the current study where such connections were less distributed through multisensory nuclei. However, the projections from multisensory nuclei in these studies was reported to be variable (Hackett et al., 2007a) or involved large injections of multiple areas (Cappe et al., 2009). Based on these results, the connections of multisensory nuclei with CL remain unclear.

Multisensory input into auditory cortex has been the focus of several studies (Falchier et al., 2002; Foxe et al., 2002; Rockland and Ojima, 2003; Murray et al., 2005; Cappe and Barone, 2005; Lakatos et al., 2007; Cappe et al., 2009) yet most of the recent attention regarding somatosensory and auditory responses in auditory cortex has focused on the medial belt area CM (Robinson and Burton, 1980a, b; Schroeder et al., 2001; Schroeder and Foxe, 2002; Fu et al., 2003; Kayser et al., 2005); however, there is also support for convergence of these modalities in the lateral belt (Kayser et al., 2005). While the projections to CL from multisensory nuclei remain unclear, somatosensory responses in the absence of these connections, as revealed from this study, is consistent with the idea that Ri is the most likely source of somatosensory input to the caudal belt areas (de la Mothe et al., 2006a; de la Mothe et al., 2012). Because there is lack of physiological studies examining somatosensory responses in the caudal lateral belt, additional studies are required to resolve whether the caudal areas of both the medial and lateral belt are responsive to auditory and somatosensory stimulation and the exact nature of the multisensory inputs to the caudal lateral belt.

In this study, topographic differences in the projections to caudal and rostral parabelt were based on the relative distribution of cells, because injections into both areas involved mainly the same nuclei (MGpd, MGm, Sg, Lim, PM). The distribution shifted from a profile characterized by strong inputs from the MGpd rostrally to one dominated by the multisensory nuclei (Sg, Lim, Po) caudally. The tendency of multisensory nuclei to be more strongly connected with caudal auditory areas is consistent with earlier studies of the medial belt, and the core regions in marmosets and macaques (de la Mothe et al., 2006b; Hackett et al., 2007a, b). This suggests the possibility that multisensory influences are greater among the caudal areas of auditory cortex. Physiological support for this notion can be found in a recent imaging study of macaque monkeys in which audiovisual convergence was restricted to the caudal areas of the core, belt, parabelt, and superior temporal sulcus (Kayser et al., 2005, 2007, 2009).

Consistency With the Working Model of Auditory Cortex

The lateral belt received input preferentially from one of the dorsal divisions of MGd (MGad, MGpd) as well as MGm, consistent with what has previously been reported in other primates (Morel and Kaas, 1992; Pandya et al., 1994; Molinari et al., 1995). In addition, rostrocaudal topography was revealed within MGd: rostral areas were preferentially connected with MGpd and caudal areas with MGad consistent with previous findings (Burton and Jones, 1976; Morel and Kaas, 1992; Pandya et al., 1994; Molinari et al., 1995). While some differences between the medial and lateral belt were noted, in general the organization of the medial and lateral belt areas appears to be similar, comprising a secondary belt region of auditory cortex that receive projections primarily from the dorsal divisions of the MGC (MGad, MGpd).

The parabelt also received input from MGpd and MGm, while there were relatively sparse connections revealed from MGv to either the lateral belt or parabelt. The lack of MGv input, which is characteristic of the primary core areas, is consistent with a hierarchical model in which the belt and parabelt regions are positioned at higher levels than the core. The dependence of the parabelt on inputs from the belt region, as found in the companion report (de la Mothe et al., 2012), supports previous conclusions that place the parabelt at a third level of processing above the belt region. Further support for positioning the parabelt at a higher stage was provided in this report from the additional inputs it received from the associative thalamic nucleus, PM. Thus, the combined results from these studies provide additional support for a core, belt, and parabelt system of organization in the primate auditory cortex.

Acknowledgements

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED

The authors acknowledge C.R. Camalier for helpful comments on the manuscript.

LITERATURE CITED

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgements
  8. LITERATURE CITED