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Connections of Auditory Medial Belt Cortex in Marmoset Monkeys

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Connections of Auditory Medial Belt Cortex in Marmoset Monkeys CONNECTIONS OF AUDITORY MEDIAL BELT CORTEX IN MARMOSET MONKEYS By Lisa de la Mothe Thesis Submitted to the Faculty of the Graduate School of Vanderbilt University in partial fulfillment of the requirements for the degree of MASTER OF ARTS in Psychology August, 2006 Nashville, Tennessee Approved: Jon Howard Kaas Troy Alan Hackett TABLE OF CONTENTS Page LIST OF TABLES…………………………………………………………………………………………..iii LIST OF FIGURES………………………………………………………………………………………...iv LIST OF ABBREVIATIONS………………………………………………………………………………..v Chapter I. INTRODUCTION…………………………………………………………………………………1 II. METHOD General Procedures………………………………………………………………………....5 Data Analysis…………………………………………………………………………………7 Auditory Stimulation………………………………………………………………………..12 Data Acquisition and Analysis….……………………………..…………………………..13 III. RESULTS Architecture………...…………………………………………………………………..15 Neuron Response Properties………………...………………………………………16 Connection Patterns…………………...……………………………………………...17 IV. DISCUSSION……………………………………………...…………………………………….23 REFERENCES………………………………………………………..…………………………………..28 ii LIST OF TABLES Table Page 1. Summary of marmoset cases, injections made and tracers used…………………………..5 iii LIST OF FIGURES Figure Page 1. Schematic drawing of the current model of auditory cortical processing…………………1 2. Photo of the retraction procedure of the parietal cortex……………………………………7 3. Image of recordings showing the tonotopic map of the left hemisphere of the marmoset auditory cortex……………………………………………………………………...8 4. Image of recordings showing the tonotopic map of the right hemisphere of the marmoset auditory cortex……………………………………………………………………...9 5. Architecture of rostral sections of the marmoset auditory cortex showing locations of borders in relation to the specific stain or reaction………………………….10 6. Architecture of caudal sections of the marmoset auditory cortex showing locations of borders in relation to the specific stain or reaction………………………….11 7. Composit of a series of sections illustrating the distribution of label through the rostral caudal extent of the auditory cortex from an injection into RM…………………..12 8. Frequency response area of an electrode penetration into the core……………………16 9. Frequency response area of an electrode penetration into the belt…………………….17 10. Schematic of the summary of connections from the RM injection………………………18 11. Examples of labeling in the medial portion of the core……………………………………19 12. Schematic of the summary of connections from the lateral belt injection………………19 13. Schematic of the summary of connections from the core injection……………………..20 14. Images of thalamic labeling from RM and CM injections…………………………………21 15. Images of anterograde banding in the lateral belt…………………………………………24 16. Images of injections into somatosensory cortex and auditory cortex……………………25 iv LIST OF ABBREVIATIONS A1 primary auditory field/ auditory area 1 AL anterolateral belt area AS arcuate sulcus BDA biotinylated dextroamine BF best frequency CF characteristic frequency CiS circular sulcus CL caudolateral belt area CM caudomedial belt area CPB caudal parabelt CS central sulcus CTB cholera toxin-B D doral division of the medial geniculate complex DY diamidino yellow FB fast blue FE fluoroemerald FR fluororuby FRA frequency response area ILS inferior limiting sulcus INS insula IPS intraparietal sulcus Lim limitans LS lateral sulcus LuS lunate sulcus M magnocellualr division of the medial geniculate complex MD medial dorsal nucleus MGC medial geniculate complex MGd dorsal division of the medial geniculate MGm magnocellular division of the medial geniculate MGv ventral division of the medial geniculate ML middle lateral belt area Po posterior group Pro proisocortex proA prokoniocortical area PS principal sulcus Pv parvalbumin R rostral area reIt retroinsular temporal cortex RL rostolateral field RM rostromedial belt area RPB rostral parabelt RT rostrotemporal area RTL rostrotemporal lateral belt area RTM rostrotemporal medial belt area S2 somatosensory area 2 Sg suprageniculate STG superior temporal gyrus STS superior temporal sulcus V ventral division of the medial geniculate complex VP ventroposterior nucleus v CHAPTER I INTRODUCTION Current models of auditory cortex organization in primates emphasize the Old World macaque monkey, but are also reinforced by comparative observations in several New World species, including marmoset, owl, and squirrel monkeys. Based on the collective findings of the field the current working model divides the auditory cortex into three levels of processing which include a primary core region, a secondary belt region and a third level of processing in the parabelt region (Figure 1). A fourth level of processing is also thought to exist, which encompasses connections to the superior temporal sulcus, rostral superior temporal gyrus, and prefrontal cortex (Kaas & Hackett, 2000). 1 Figure 1. Diagram of current auditory processing model. The core region is subdivided into three areas, A1, R and RT, which can be identified by architectonic characteristics typical of primary sensory areas including; koniocortical cytoarchitecture, dense astriate myelination, as well as dense expression of acetylcholinesterase, cytochrome oxidase, and parvalbumin (Morel &Kaas, 1992, Hackett et al., 1998). All areas of the core receive independent parallel inputs from the ventral medial geniculate (MGv) and thus process information in parallel (Rauschecker et. al 1997). The core areas are cochleotopically organized by characteristic frequency with isorepresentation curved. In A1 the low frequency representation is rostral and the high frequency representation caudal (Figure 1) (Kaas & Hackett, 1998; Kaas and Hackett, 2000). This gradient is reversed in R which shares a low frequency border with A1 and a high frequencies border with RT. The core areas project primarily to the belt areas where strongest connections are between adjacent areas and only weak projections to the parabelt (Hackett et al., 1998). Surrounding the core both medially and laterally is the belt region which is divided into seven or more areas. Some of those areas are distinguished on the basis of physiological profiles and connection patterns (CL, ML, AL, CM), while others are based solely on connection patterns (RM, RTM, RTL). Medially to the core lie areas CM, RM, and RTM. Areas CL, ML, AL, and RTL border the core laterally. The belt has been shown to have strong interconnections with the core as well as other belt areas (Merzenich & Brugge 1973, Atkin et al. 1988, Morel & Kaas 1992). Thalamic connections to the belt areas come from the dorsal (MGd) and the magnocellular (MGm) divisions of the medial geniculate body, however, it appears to depend on the core for activation from cortical inputs (Kaas & Hackett, 2000). Projections from the belt area distribute principally to the parabelt (Kaas & Hackett,1998). The lateral belt areas are the most well studied and respond better to narrow bands than pure tones (Rauschecker et al. 1995). This preference for more complex stimuli is thought to apply to the medial belt areas (Rauschecker et al., 1997), but the location deep within the lateral sulcus has made this region difficult to study. The parabelt is located lateral to the lateral belt on the dorsal surface of the superior temporal gyrus and receives strong projections from the belt areas (Kaas & Hackett 1998). Those caudal 2 belt areas that border A1 project to the caudal parabelt, whereas the rostral areas bordering R and RT project to the rostral parabelt (Kaas & Hackett, 1998). Area RM in the belt appears to be the only area that does not follow this rostral caudal topography as it projects to both rostral and caudal divisions of the parabelt, (Kaas & Hackett 1998). Thalamic connections of the parabelt include the MGd and MGm as well as the suprageniculate/limitans (Sg) and the medial pulvinar nuclei (Hackett et al. 1998b). There are no projections from the MGv or the core area (Hackett et al. 1998) and thus the parabelt receives auditory input either through thalamic projections from non-primary nuclei or more from the belt areas. The cortical connection patterns place the parabelt at a third level of processing (Kaas & Hackett 1998). In our working model of auditory cortex organization, the anatomical and physiological properties of the belt areas medial to the core are the least well understood due in part to the narrow width of these areas, and their location deep within the lateral sulcus which presents numerous experimental challenges. Accordingly, the connections of the medial belt fields are only partially known from tracer injections made in other cortical fields. The principle aim of the present study was refinement of the working model with respect to the contribution of medial belt areas, which appear to be functionally distinct from lateral belt areas (Jones & Burton, 1976; Schroeder et al., 2001), but has not yet been systematically studied in any primate. Recent physiological evidence suggests that there may be auditory and somatic sensory convergence in at least one medial belt area, CM, (Schroeder et al., 2001), but a source of somatic sensory input to CM has not been identified. Although the medial belt is situated between primary auditory and secondary somatic sensory cortex (e.g., S2), projections from somatic sensory cortex are not known to target the medial belt. In the absence of somatic sensory cortical inputs, one hypothesis is that multisensory or somatic nuclei in the thalamus may drive responses to somatic stimulation in the medial belt. A subcortical
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