Catherine G. Cusick

Cortical connections of area 18 and dorsolateral visual cortex in squirrel monkeys

Cortical connections of area 18 (V-II) and part of the dorsolateral visual area (DL) were determined in squirrel monkeys with single and multiple injections of the sensitive bidirectional tracer, wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). Injections were placed into portions of area 18 or DL on the dorsolateral surface of the brain, patterns of label were examined in brain sections cut parallel to the surface of physically flattened cortex, and comparisons were made with alternate brain sections reacted for cytochrome oxidase (CO) or stained for myelinated fibers. Major results are as follows. (1) Area 18 was identified by a characteristic alternation of dense and light CO bands crossing its width; the middle temporal visual area (MT) was CO dense; the dorsolateral area (DL) was less reactive, with rostral DL (DLR) lighter than caudal DL (DLC); area 17 had clear CO puffs in the supragranular layers. (2) Intrinsic connections revealed in area 18 included a narrow 100-200 microns fringe of less dense label around each injection core, label unevenly distributed in small clumps within 1-2 mm of injection sites, and clumps of transported label up to 6 mm from injection sites. (3) Single and multiple injections in area 18 produced patterns of labeled cells and terminations in area 17 that ranged from lattice- to puff-like in surface-view distribution. With multiple area 18 injections, regions of area 17 could be found where transported label was concentrated in CO puffs, avoided the CO puffs, or overlapped both puff and interpuff divisions of cortex. The labeled regions of area 17 were somewhat larger than the injection sites, suggesting some convergence from area 17 to area 18. (4) The major rostral connections of area 18 were with caudal DL (DLC). Rostral DL (DLR) was largely free of transported label. Single injection sites in area 18 resulted in several large clumps of label separated by regions of sparse or no label in DLC. Injections in lateral area 18 produced lateral foci of label in DL, while more medial injections produced more medial foci. However, following multiple injections into area 18 that included the representation of central vision, a continuous 2-3-mm-wide band of infragranular labeled cells extended from area 18 caudally to MT rostrally in the presumed location of central vision in DLC and DLR. (5) Injections in area 18 produced foci of label in MT. Label was more dorsal in MT with more dorsal injection sites in area 18.(ABSTRACT TRUNCATED AT 400 WORDS)

Neurochemical and connectional organization of the dorsal pulvinar complex in monkeys

To investigate the organization of the dorsal pulvinar complex, patterns of neurochemical staining were correlated with cortico‐pulvinar connections in macaques (Macaca mulatta). Three major neurochemical subdivisions of the dorsal pulvinar were identified by acetylcholinesterase (AChE) histochemistry, as well as immunostaining for calbindin‐D28K and parvalbumin. The dorsal lateral pulvinar nucleus (PLd) was defined on histochemical criteria as a distinct AChE‐ and parvalbumin‐dense, calbindin‐poor wedge that was found to continue caudally along the dorsolateral edge of the pulvinar to within 1 mm of its caudal pole. The ventromedial border of neurochemical PLd with the rest of the dorsal pulvinar, termed the medial pulvinar (PM), was sharply defined. Overall, PM was lighter than PLd for AChE and parvalbumin and displayed lateral (PMl) and medial (PMm) histochemical divisions. PMm contained a central “oval” (PMm‐c) that stained darker for AChE and parvalbumin than the surrounding region. The neurochemically defined PLd was labeled by tracer injections in the inferior parietal lobule (IPL) and dorsolateral prefrontal cortex but not the superior temporal gyrus (STG). Label within PMl was found after prefrontal and IPL and, to a lesser extent, after STG injections. The PMm was labeled after injections of the IPL and STG, but only sparsely following prefrontal injections. The histochemically distinct subregion or module of PMm, PMm‐c, was labeled only by STG injections. Overlapping labeling was found in dorsal pulvinar divisions PMl and PLd following paired IPL/prefrontal, but not IPL/STG or these particular STG/prefrontal, injections. Thus, PLd may be a visuospatially related region whereas PM appears to contain several types of territories, some related to visual or auditory inputs, and others that receive directly converging input from posterior parietal and prefrontal cortex and may participate in a distributed cortical network concerned with visuospatial functions. J. Comp. Neurol. 419:61–86, 2000.

Architectonics and cortical connections of the upper bank of the superior temporal sulcus in the rhesus monkey: An analysis in the tangential plane

Area TPO in the upper bank of the superior temporal sulcus (STS) of macaque monkeys is thought to correspond to the superior temporal polysensory (STP) cortex, but has been shown to have neurochemical/connectional subdivisions. To examine directly the relationship between chemoarchitecture and cortical connections of area TPO, the upper bank of the STS was sectioned tangential to the cortical surface. Three subdivisions of area TPO (TPOr, TPOi, and TPOc) were examined with cytochrome oxidase (CO) histochemistry and neurofilament protein (NF) immunoreactivity and architectonic patterns were compared with connections on the same or adjacent sections. Area TPOc, which may partly overlap with the location of the medial superior temporal area MST, exhibited regular patchy staining for CO in layers III/IV and a complementary pattern in the NF stain. Area TPOr, but not TPOi, also had a patchy pattern of complementary staining in CO and neurofilament similar to TPOc, although not as distinct. Tracer injections within cortex including the frontal eye fields (areas 46 and 8) labeled areas TPOc, TPOi, and TPOr. The caudal inferior parietal lobule (IPL) projected to all three areas. The projections from prearcuate and posterior parietal cortices showed both overlap and nonoverlap with each other within TPOc, TPOi, and TPOr. Projections were to all neurochemical components within the subdivisions of TPO. The findings support the parcellation of area TPO into three subdivisions and extend findings of chemoarchitectonic modules within high‐order association cortices. J. Comp. Neurol. 467:418–434, 2003.

The Superior Temporal Polysensory Region in Monkeys

This chapter will review the progressive refinement of the concept of superior temporal polysensory (STP) cortex in macaque monkeys, describe the different organizational schemes in current use, and highlight a number of unresolved issues. Studies of the STP region have been limited by the difficulty of reconciling disparate physiological findings, suggesting, on the one hand, a role in visuospatial functions or eye movement control, and on the other, contributions to complex visual recognition functions. It is perhaps premature to assign STP cortex to either the dorsal or ventral stream of visual processing, thought to be crucial for visuospatial functions and object recognition, respectively, and the potential integrative functions of this region should not be ignored.

Neurochemical organization of inferior pulvinar complex in squirrel monkeys and macaques revealed by acetylcholinesterase histochemistry, calbindin and Cat‐301 immunostaining, and Wisteria floribunda agglutinin binding

To investigate whether the inferior pulvinar complex has a common organization in different primates, the chemoarchitecture of the visual thalamus was re‐examined in squirrel monkeys (Saimiri sciureus) and macaques (Macaca mulatta). The inferior pulvinar (PI) complex consisted of multiple subdivisions and encompassed the classic PI, and adjacent ventral parts of the lateral and medial pulvinar (PL and PM, respectively). In keeping with nomenclature suggested previously for macaques, the PI subdivisions were termed the posterior, medial, central, lateral, and lateral‐shell (PIP, PIM, PIC, PIL, and PIL‐S). In both species, PIP was intense for calbindin, light for acetylcholinesterase (AChE), and very light for Wisteria floribunda agglutinin (WFA) histochemistry. The PIM was calbindin poor, AChE rich, and moderate for WFA. The PIC was calbindin intense, lighter for AChE, and exhibited little WFA binding. PIL and PIL‐S contained populations of large calbindin or WFA cells that were more numerous in PIL‐S. Although staining with the monoclonal antibody Cat‐301 differed between macaques and squirrel monkeys, the same subdivisions were displayed. Moderately dense, patchy Cat‐301 stain was found in PIM of macaques, whereas in squirrel monkeys PIM was light. Connections of the rostral dorsolateral (DLr) and middle temporal (MT) areas of visual cortex in squirrel monkeys were compared with PI subdivisions revealed by the newer histochemical methods in the same cases. The major connections of DLr were with PIC and of MT were with PIM. J. Comp. Neurol. 409:452–468, 1999.

Neural hybrid model of semantic object memory: Implications from event-related timing using fMRI

Previous studies by our group have demonstrated fMRI signal changes and synchronized gamma rhythm EEG oscillations between thalamus and cortical regions as subjects recall objects from visually presented features. Here, we extend this work by estimating the time course of fMRI signal changes in the cortical and subcortical regions found to exhibit evidence for task-related activation. Our results indicate that there are separate loci of signal changes in the thalamus (dorsomedial and pulvinar) that exhibit notable differences in times of onset, peak and return to baseline of signal changes. The signal changes in the pulvinar demonstrate the slowest transients of all the cortical and subcortical regions we examined. Evaluation of cortical regions demonstrated salient differences as well, with the signal changes in Brodmann area 6 (BA6) rising, peaking, and returning to baseline earlier than those detected in other regions. We conclude that BA6 mediates early designation or refinement of search criteria, and that the pulvinar may be involved in the binding of feature stimuli for an integrated object memory.

Effects of chronic monocular enucleation on calcium binding proteins calbindin-D28k and parvalbumin in the lateral geniculate nucleus of adult rhesus monkeys

The calcium binding proteins parvalbumin and calbindin-D28k were localized immunocytochemically within the lateral geniculate nucleus of adult monkeys at 1-7 months after monocular enucleation. Within the deafferented magno- and parvocellular layers, parvalbumin and calbindin-D28k immunoreactive fibers were depleted at all post-enucleation times. The neuronal staining for parvalbumin was similar in numerical density and intensity between the deafferented and intact layers. In hemispheres examined at 5 and 7 months post-enucleation, parvalbumin-immunoreactive fibers were also lost within the deprived ocular dominance bands in layers IVA, IVC and VI of the visual cortex, suggesting that cellular expression or axonal transport of parvalbumin may be decreased in the deafferented geniculate laminae. While the intact magno- and parvocellular layers contained very few neurons that were immunoreactive for calbindin-D28k, the density of calbindin-D28k-positive neurons increased in these layers after deafferentation. The counts of calbindin-D28k and parvalbumin immunostained neurons were not statistically different at 4-7 months post-enucleation. Because virtually all magno- and parvocellular projection neurons express parvalbumin, many parvalbumin neurons that normally do not contain calbindin-D28k may co-express this in response to injury. The findings suggest that long-term deafferentation imposes additional calcium buffering requirements on lateral geniculate neurons.

Chapter 1: Anatomical organization of the superior colliculus in monkeys: corticotectal pathways for visual and visuomotor functions

Publisher Summary The purpose of this chapter is to discuss aspects of the anatomical organization of the superior colliculus in monkeys. The chapter also attempts to relate dual collicular functions to afferents from cortical visual and visuomotor systems. The superior colliculus has important links with systems for both visual perception and visuomotor functions. The anatomical basis for dual functions of the superior colliculus appears to lie in the well-documented connectional differences between the superficial and deep collicular compartments. Much progress has recently been made in the understanding of the numbers and interconnections of separate cortical areas, and more sensitive anatomical methods have permitted refinements in some of the observations on corticotectal projections. Projections of both posterior parietal and inferotemporal cortex appear to be mainly to the deeper layers, as are inputs from visuomotor areas of cortex. Thus, collicular visual and visuomotor compartments are closely linked with cortical perceptual and motor systems, respectively. In addition, the chapter also presents the new findings on visual corticotectal projections in squirrel monkeys.

Subdivisions of the motor and somatosensory thalamus of primates revealed with Wisteria floribunda agglutinin histochemistry

We obtained well-differentiated staining of thalamic subdivisions in rhesus macaques and squirrel monkeys using a lectin, Wisteria floribunda agglutinin (WFA), that labels extracellular matrix proteoglycans. Regional variations in staining were observed within the motor and somatosensory thalamic regions that bear on current interpretations of the organization of these regions. The pattern of WFA staining was generally similar to that obtained with Cat-301 antibody, which also stains proteoglycans. However, WFA reliably produced selective staining in both squirrel monkeys and macaques, whereas Cat-301 stained macaques more consistently than squirrel monkeys.

Neurochemical organization of chimpanzee inferior pulvinar complex.

The pulvinar of primates, which connects with all visual areas, has been implicated in visual attention and in control of eye movements. Recently, five separate neurochemical subdivisions of a region termed the inferior pulvinar complex have been identified in monkeys (Gray et al. [ 1999 ] J Comp Neurol 409:452–468; Gutierrez et al. [ 1995 ] J Comp Neurol 363:545–562), and comparable subdivisions have been mapped in humans (Cola et al. [ 1999 ] NeuroReport 10:3733–3738). In the present study, we investigated the inferior pulvinar of the chimpanzee (Pan troglodytes), the closest evolutionary relative of humans, using cytochrome oxidase (CO) and acetylcholinesterase (AChE) histochemistry, and immunocytochemistry for calbindin. Each staining method demarcated five histochemical zones corresponding, from medial to lateral, to the posterior (PIP), medial (PIM), central PIC), lateral (PIL), and the lateral‐shell (PIL‐S) divisions in monkeys. The PIP division stained darkly for calbindin and lightly for CO and AChE. The PIM division was characterized by less neuropil staining for calbindin, and by distinct, intensely stained patches of CO and AChE. PIC appeared lighter than adjacent divisions with CO and AChE histochemistry and was moderately stained with calbindin. PIL was moderately to darkly stained with each method and was adjoined by a lighter staining shell, PIL‐S. Thus, in the aspects of organization we examined, the inferior pulvinar of chimpanzees closely resembles that of humans and monkeys. This investigation provides a foundation for more detailed studies of the thalamic relationships of extrastriate cortex in apes and humans. J. Comp. Neurol. 484:299–312, 2005.