Neurofilament protein distribution in the macaque monkey dorsolateral premotor cortex

Abstract

Regional and laminar distribution patterns of neurofilament proteins in the dorsolateral premotor cortex (PMd) were studied with monoclonal antibody SMI-32 in five adult macaque monkeys and compared with the cytoarchitectonical features of the PMd. Our goal was to reveal whether the increasing functional diversity of the PMd which electrophysiological studies have unravelled over the last years is reflected on a structural level by differences in the neurochemical phenotype. Differences in size, shape and packing density of immunopositive layer III and V pyramidal cells define areas much more clearly than do differences in cytoarchitecture. The PMd can be subdivided into a rostral and a caudal part at a level slightly anterior to the genu of the arcuate sulcus. The extent of these two areas matches the two cytoarchitectonically defined areas F7 and F2, respectively. Within area F2, differences in layer V immunoreactive neurons define a dorsal (F2d) and a ventral (F2v) region. The border between areas F2d and F2v lies at the superior precentral dimple and cannot be detected cytoarchitectonically in Nissl-stained sections. Neurofilament proteins are involved in the stabilization of the cytoskeleton of the axon and have been correlated with axonal size and conduction velocity of nerve fibres. This regional variability in the neurochemical phenotype of layer V within the caudal PMd may reflect a differential organization of the descending output from this part of the premotor cortex. It might also be related to differences in the motor control of voluntary arm and leg movements.

Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans

“…In each stained neuron, an apical dendrite could be observed ascending towards layer I, as well as several horizontally-oriented basal dendrites. Similar to other studies of NPNFP staining in area 4 of macaques, chimpanzees, and humans [Baleydier et al, 1997;Preuss et al, 1997;Gabernet et al, 1999;Qi et al, 1999;Geyer et al, 2000], two prominent bands of immunoreactive tissue spanning layers III and V were apparent ( fig. 2).…”

“…Because the distribution of NPNFP-ir cells reflects regional specializations of pyramidal neurons, regional variation in the staining of NPNFP-ir elements facilitates more clear and consistent parcellation of cortical areas. Studies of NPNFP staining have described regional variation in the neocortex of dogs [Hof et al, 1996a], visual cortex of cats [van der Gucht et al, 2001], macaque monkeys [Hof and Morrison, 1995] and vervet monkeys [Chaudhuri et al, 1996], premotor and motor cortices of macaques [Preuss et al, 1997;Gabernet et al, 1999;Geyer et al, 2000] and humans [Baleydier et al, 1997], superior temporal cortex of macaques [Cusick et al, 1995], inferior frontal cortex of chimpanzees [Sherwood et al, 2003a], and cingulate and orbitofrontal cortices of macaques and humans [Hof and Nimchinsky, 1992;Carmichael and Price, 1994;Hof et al, 1995a;Nimchinsky et al, 1997].…”

“…In the present study, estimates of NPNFP-ir neuron proportions were obtained by sampling within two zones corresponding to the deep portions of layer III (i.e., layer IIIb/c) and layer V (i.e., layer Vb). Because the highest density of NPNFP staining typically occurs in these sublayers [Baleydier et al, 1997;Preuss et al, 1997;Gabernet et al, 1999;Qi et al, 1999;Geyer et al, 2000], a more restricted laminar analysis was pursued in order to enhance sensitivity to interspecific differences. A major finding of the present study was that the frequency of NPNFP-ir neurons in layers IIIb/c and Vb of area 4 evinces a striking increase from Old World monkeys to 98 Brain Behav Evol 2004;63:82-106 Sherwood/Holloway/Erwin/Hof hominids, with a relatively greater proportion of NPNFPir neurons in African great apes and humans compared to orang-utans.…”

Cyto- and Chemoarchitecture of the Cortex of the Tammar Wallaby <i>(Macropus</i><i>eugenii)</i>: Areal Organization

“…The distribution of SMI-32 immunoreactive neurons in supra-and infragranular bands in tammar wallaby V1 with no immunoreactivity in layer IV is similar to the pattern of immunoreactivity noted in cat primary and secondary visual cortex [areas 17 and 18;van der Gucht et al, 2001]. On the other hand, we did not fi nd any bilaminar distribution of SMI-32 immunoreactive somata in regions of cortex where these are common in eutheria [e.g., dorsolateral premotor cortex and motor cortex; Preuss et al, 1997;Gabernet et al, 1999;Geyer et al, 2000] and we could not differentiate the motor cortex into separate regions on the basis of SMI-32 immunoreactivity, as has been done for the macaque precentral cortex [Preuss et al, 1997]. Nevertheless, the presence of a bilaminar distribution of SMI-32 + neurons in anterodorsal Cg suggests a separate limbic functional area in that part of the cortical mantle, which might engage in long-distance association connections with other parts of the cortex.…”

Microcircuitry of Agranular Frontal Cortex: Testing the Generality of the Canonical Cortical Microcircuit

“…Areas outlined in blue are magnified at right. V1 can be clearly delineated by laminae and shows a distinct layer IV separating layers III and V. In contrast, SEF exhibits clusters of pyramidal cells in layer III with less dense pyramidal cells in layer V (Geyer et al, 2000). b, Comparison of laminar distribution of acetylcholinesterase (AChE), myelin fibers, and Nissl substance in primary visual cortex (top) and SEF (bottom).…”