Neurochemical, morphologic, and laminar characterization of cortical projection neurons in the cingulate motor areas of the macaque monkey

Abstract

The primate cingulate gyrus contains multiple cortical areas that can be distinguished by several neurochemical features, including the distribution of neurofilament protein-enriched pyramidal neurons. In addition, connectivity and functional properties indicate that there are multiple motor areas in the cortex lining the cingulate sulcus. These motor areas were targeted for analysis of potential interactions among regional specialization, connectivity, and cellular characteristics such as neurochemical profile and morphology. Specifically, intracortical injections of retrogradely transported dyes and intracellular injection were combined with immunocytochemistry to investigate neurons projecting from the cingulate motor areas to the putative forelimb region of the primary motor cortex, area M1. Two separate groups of neurons projecting to area M1 emanated from the cingulate sulcus, one anterior and one posterior, both of which furnished commissural and ipsilateral connections with area M1. The primary difference between the two populations was laminar origin, with the anterior projection originating largely in deep layers, and the posterior projection taking origin equally in superficial and deep layers. With regard to cellular morphology, the anterior projection exhibited more morphologic diversity than the posterior projection. Commissural projections from both anterior and posterior fields originated largely in layer VI. Neurofilament protein distribution was a reliable tool for localizing the two projections and for discriminating between them. Comparable proportions of the two sets of projection neurons contained neurofilament protein, although the density and distribution of the total population of neurofilament protein-enriched neurons was very different in the two subareas of origin. Within a projection, the participating neurons exhibited a high degree of morphologic heterogeneity, and no correlation was observed between somatodendritic morphology and neurofilament protein content. Thus, although the neurons that provide the anterior and posterior cingulate motor projections to area M1 differ morphologically and in laminar origin, their neurochemical profiles are similar with respect to neurofilament protein. This suggests that neurochemical phenotype may be a more important unifying feature for corticocortical projections than morphology.

Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32

“…These studies have utilized a wide range of species including humans (Campbell and Morrison, 1989;Hof et al, , 1995aDel Rio and DeFelipe, 1994;Vogt et al, 2001), old-world monkey (Campbell and Morrison, 1989;Hof and Nimchinsky, 1992;Hof and Morrison, 1995;Hof et al, 1995b;Cusick et al, 1995;Nimchinsky et al, 1996;Preuss et al, 1997;Lewis and Van Essen, 2000;Suzuki and Amaral, 2003;Luppino et al, 2005;Saleem et al, 2007), new-world-monkey (Chaudhuri et al, 1996;Duffy and Livingstone, 2003;Baldauf, 2005;Soares et al, 2008), cat (Kaneko et al, 1994;Van der Gucht et al, 2001, 2005, dog , dolphin , grey squirrel (Wong and Kaas, 2008), hamster (Boire et al, 2005), echidna (Hassiotis et al, 2004(Hassiotis et al, , 2005 and gerbil (Budinger et al, 2000). Across all species examined, large and medium size pyramidal cells are by far the most frequently reactive neuronal types.…”

“…16). By using the properties of non-phosphorylated epitopes found throughout cortical (Campbell and Morrison, 1989;Hof et al, 1995b;Nimchinsky et al, 1996;Van der Gucht et al, 2001;Boire et al, 2005) and subcortical (Bickford et al, 1998;Van der Gucht et al, 2001;Boire et al, 2005) structures, SMI-32 has proven to be a very powerful tool for determining functional borders.…”

Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey

“…SMI-32ir displays specific regional and laminar distribution patterns and is an effective architectonic tool in the macaque for the delineation of occipito-parietal (e.g., Hof and Morrison 1995), temporal (Cusick et al 1995), agranular frontal (e.g., Geyer et al 2000), cingulate (Nimchinsky et al 1996) and prefrontal (Carmichael and Price 1994) areas. We found SMI-32ir very helpful for a precise delineation and further characterization of the different caudal VLPF areas.…”

Cytoarchitecture of the mouse neocortex revealed by the low-molecular-weight neurofilament protein subunit

“…This neurochemical distinction could turn out functionally important when comparing labeling patterns across species and in studies of the proportion of NFP-containing neurons in pathways (Campbell et al 1991;Hof et al , 1997Nimchinsky et al 1996). The relationship between NFP content and myelination was already presented by other authors who associated NFP labeling and cortical neuron size and clarified the regulatory role of myelination in neurofilament phosphorylation state (Campbell and Morrison 1989;de Waegh et al 1992;Hayes and Lewis 1992;Cole et al 1994;Gotow 2000).…”

“…The non-pyramidal neuronal population that contains NFPs Brain Struct Funct (2011) 216:183-199 195 includes most likely star pyramids (Peters and Kara 1985;Cipolloni and Pandya 1991;Martínez-García et al 1994; Van der Gucht et al 2007). Previous studies on carnivores and primates located SMI-32 exclusively in a subset of pyramidal neurons known to be a class of long association projection neurons (Hof et al , 1996cNimchinsky et al 1996; Van der Gucht et al 2001. Various combinations of all the NF-L immunoreactivity features clearly typified distinct cortical areas and allowed to differentiate three different types of topographical boundaries in the mouse brain categorized as definite, definable, and transitional borders (see also Table 2).…”