Cell and neuron densities vary across the cortical sheet in a predictable manner across different primate species (Collins et al., 2010b). Primary motor cortex, M1, is characterized by lower neuron densities relative to other cortical areas. M1 contains a motor representation map of contralateral body parts from tail to tongue in a mediolateral sequence. Different functional movement representations within M1 likely require specialized microcircuitry for control of different body parts, and these differences in circuitry may be reflected by variation in cell and neuron densities. Here we determined cell and neuron densities for multiple sub-regions of M1 in six primate species, using the semi-automated flow fractionator method. The results verify previous reports of lower overall neuron densities in M1 compared to other parts of cortex in the six primate species examined. The most lateral regions of M1 that correspond to face and hand movement representations, are more neuron dense relative to medial locations in M1, which suggests differences in cortical circuitry within movement zones.
M1; flow fractionator; isotropic fractionator; movement
Inferences about how the complex sensory and motor systems of the human brain evolved are based on the results of comparative studies of brain organization across a range of mammalian species, and evidence from the endocasts of fossil skulls of key extinct species. The endocasts of the skulls of early mammals indicate that they had small brains with little neocortex. Evidence from comparative studies of cortical organization from small-brained mammals of the six major branches of mammalian evolution supports the conclusion that the small neocortex of early mammals was divided into roughly 20–25 cortical areas, including primary and secondary sensory fields. In early primates, vision was the dominant sense, and cortical areas associated with vision in temporal and occipital cortex underwent a significant expansion. Comparative studies indicate that early primates had 10 or more visual areas, and somatosensory areas with expanded representations of the forepaw. Posterior parietal cortex was also expanded, with a caudal half dominated by visual inputs, and a rostral half dominated by somatosensory inputs with outputs to an array of seven or more motor and visuomotor areas of the frontal lobe. Somatosensory areas and posterior parietal cortex became further differentiated in early anthropoid primates. As larger brains evolved in early apes and in our hominin ancestors, the number of cortical areas increased to reach an estimated 200 or so in present day humans, and hemispheric specializations emerged. The large human brain grew primarily by increasing neuron number rather than increasing average neuron size.
The visual pulvinar is part of the dorsal thalamus, and in primates it is especially well developed. Recently, our understanding of how the visual pulvinar is subdivided into nuclei has greatly improved as a number of histological procedures have revealed marked architectonic differences within the pulvinar complex. At the same time, there have been unparalleled advances in understanding of how visual cortex of primates is subdivided into areas and how these areas interconnect. In addition, considerable evidence supports the view that the hierarchy of interconnected visual areas is divided into two major processing streams, a ventral stream for object vision, and a dorsal stream for visually guided actions. In this review, we present evidence that a subset of medial nuclei in the inferior pulvinar function predominantly as a subcortical component of the dorsal stream while the most lateral nucleus of the inferior pulvinar and the adjoining ventrolateral nucleus of the lateral pulvinar are more devoted to the ventral stream of cortical processing. These nuclei provide cortico-pulvinar-cortical interactions that spread information across areas within streams, as well as information relayed from the superior colliculus via inferior pulvinar nuclei to largely dorsal stream areas.
visual system; superior colliculus; visual cortex; thalamus
After 100 years of progress in understanding the organization of cerebral cortex, three issues have persisted over the last 35 years, which are revisited in this paper. First, is V3 an established or questionable area of visual cortex? Second, does taste cortex include part of area 3b (S1 proper) and other somatosensory areas? Third, is primary auditory cortex, A1, of primates the homologue of A1 in cats? The existence of such questions about even the early stages of cortical processing reflects the difficulties in mapping cerebral cortex, and reminds us that the era of basic discovery is far from over.
gustatory cortex; V3; auditory cortex; somatosensory cortex; visual cortex
Currently, we lack consensus regarding the organization along the anterior border of dorsomedial V2 in primates. Previous studies suggest that this region could be either the dorsomedial area, characterized by both an upper and a lower visual field representation, or the dorsal aspect of area V3, which only contains a lower visual field representation. We examined these proposals by using optical imaging of intrinsic signals to investigate this region in the prosimian galago (Otole-mur garnettii). Galagos represent the prosimian radiation of surviving primates; cortical areas that bear strong resemblances across members of primates provide a strong argument for their early origin and conserved existence. Based on our mapping of horizontal and vertical meridian representations, visuotopy, and orientation preference, we find a clear lower field representation anterior to dorsal V2 but no evidence of any upper field representation. We also show statistical differences in orientation preference patches between V2 and V3. We additionally supplement our imaging results with electrode array data that reveal differences in the average spatial frequency preference, average temporal frequency preference, and sizes of the receptive fields between V1, V2, and V3. The lack of upper visual field representation along with the differences between the neighboring visual areas clearly distinguish the region anterior to dorsal V2 from earlier visual areas and argue against a DM that lies along the dorsomedial border of V2. We submit that the region of the cortex in question is the dorsal aspect of V3, thus strengthening the possibility that V3 is conserved among primates.
V3; galago; imaging; electrode; DM; orientation
Relating stimulus properties to the response properties of individual neurons and neuronal networks is a major goal of sensory research. Many investigators implant electrode arrays in multiple brain areas and record from chronically implanted electrodes over time to answer a variety of questions. Technical challenges related to analyzing large-scale neuronal recording data are not trivial. Several analysis methods traditionally used by neurophysiologists do not account for dependencies in the data that are inherent in multi-electrode recordings. In addition, when neurophysiological data are not best modeled by the normal distribution and when the variables of interest may not be linearly related, extensions of the linear modeling techniques are recommended. A variety of methods exist to analyze correlated data, even when data are not normally distributed and the relationships are nonlinear. Here we review expansions of the Generalized Linear Model designed to address these data properties. Such methods are used in other research fields, and the application to large-scale neuronal recording data will enable investigators to determine the variable properties that convincingly contribute to the variances in the observed neuronal measures. Standard measures of neuron properties such as response magnitudes can be analyzed using these methods, and measures of neuronal network activity such as spike timing correlations can be analyzed as well. We have done just that in recordings from 100-electrode arrays implanted in the primary somatosensory cortex of owl monkeys. Here we illustrate how one example method, Generalized Estimating Equations analysis, is a useful method to apply to large-scale neuronal recordings.
ANOVA; Generalized Estimating Equations; Generalized Linear Mixed Models; neuronal ensembles; multi-electrode; parallel recordings; primate
In the present study, galago brains were sectioned in the coronal, sagittal or horizontal planes, and sections were processed with several different histochemical and immunohistochemical procedures to reveal the architectonic characteristics of the various cortical areas. The histochemical methods used included the traditional Nissl, cytochrome oxidase and myelin stains, as well as a zinc stain, which reveals free ionic zinc in the axon terminals of neurons. Immunohistochemical methods include parvalbumin (PV) and calbindin (CB), both calcium-binding proteins, and the vesicle glutamate transporter 2 (VGluT2). These different procedures revealed similar boundaries between areas, which suggests that functionally relevant borders were being detected. These results allowed a more precise demarcation of previously identified areas. As thalamocortical terminations lack free ionic zinc, primary cortical areas were most clearly revealed by the zinc stain, due to the poor zinc staining of layer 4. Area 17 was especially prominent, as the broad layer 4 was nearly free of zinc stain. However, this feature was less pronounced in the primary auditory and somatosensory cortex. As VGluT2 is expressed in thalamocortical terminations, layer 4 of primary sensory areas was darkly stained for VGluT2. Primary motor cortex had reduced VGluT2 staining, and increased zinc-enriched terminations in the poorly developed granular layer 4 compared to the adjacent primary somatosensory area. The middle temporal visual (MT) showed increased PV and VGluT2 staining compared to the surrounding cortical areas. The resulting architectonic maps of cortical areas in galagos can usefully guide future studies of cortical organizations and functions.
primate; cortical areas; visual cortex; motor cortex; somatosensory cortex; auditory cortex; prosimian
Squirrels are highly visual mammals with an expanded cortical visual system and a number of well-differentiated architectonic fields. In order to describe and delimit cortical fields, subdivisions of cortex were reconstructed from serial brain sections cut in the coronal, sagittal, or horizontal planes. Architectonic characteristics of cortical areas were visualized after brain sections were processed with immunohistochemical and histochemical procedures for revealing parvalbumin, calbindin, neurofilament protein, vesicle glutamate transporter 2, limbic-associated membrane protein, synaptic zinc, cytochrome oxidase, myelin or Nissl substance. In general, these different procedures revealed similar boundaries between areas, suggesting that functionally relevant borders were being detected. The results allowed a more precise demarcation of previously identified areas as well as the identification of areas that had not been previously described. Primary sensory cortical areas characterized by sparse zinc staining of layer 4, as thalamocortical terminations lack zinc, as well as by layer 4 terminations rich in parvalbumin and vesicle glutamate transporter 2. Primary areas also expressed higher levels of cytochrome oxidase and myelin. Primary motor cortex was associated with large SMI-32 labeled pyramidal cells in layers 3 and 5. Our proposed organization of cortex in grey squirrels includes both similarities and differences to the proposed of cortex in other rodents such as mice and rats. The presence of a number of well-differentiated cortical areas in squirrels may serve as a guide to the identification of homologous fields in other rodents, as well as a useful guide in further studies of cortical organization and function.
Rodents; cortical areas; visual cortex; motor cortex; somatosensory cortex; auditory cortex; cingulate cortex; retrosplenial cortex
Tree shrews are small mammals that bear some semblance to squirrels, but are actually close relatives of primates. Thus, they have been extensively studied as a model for the early stages of primate evolution. In the present study, subdivisions of cortex were reconstructed from brain sections cut in the coronal, sagittal or horizontal planes, and processed for parvalbumin (PV), SMI-32 immunopositive neurofilament protein epitopes, vesicle glutamate transporter 2 (VGluT2), free ionic zinc, myelin, cytochrome oxidase (CO) and Nissl substance. These different procedures revealed similar boundaries between areas, suggesting the detection of functionally relevant borders and allowed a more precise demarcation of cortical areal boundaries. Primary cortical areas were most clearly revealed by the zinc stain, due to the poor staining of layer 4, as thalamocortical terminations lack free ionic zinc. Area 17 (V1) was especially prominent, as the broad layer 4 was nearly free of zinc stain. However, this feature was less pronounced in primary auditory and somatosensory, cortex. In primary sensory areas, thalamocortical terminations in layer 4 densely express VGluT2. Auditory cortex consists of two architectonically distinct subdivisions, a primary core region (Ac), surrounded by a belt region (Ab) that had a slightly less developed koniocellular appearance. Primary motor cortex (M1) was identified by the absence of VGluT2 staining in the poorly developed granular layer 4 and the presence of SMI-32 labeled pyramidal cells in layers 3 and 5. The presence of well-differentiated cortical areas in tree shrews indicates their usefulness in studies of cortical organization and function.
Rodents; primates; cortical areas; visual cortex; motor cortex; somatosensory cortex; auditory cortex; cingulate cortex; retrosplenial cortex; insular cortex
Brain size scales as different functions of its number of neurons across mammalian orders such as rodents, primates, and insectivores. In rodents, we have previously shown that, across a sample of 6 species, from mouse to capybara, the cerebral cortex, cerebellum and the remaining brain structures increase in size faster than they gain neurons, with an accompanying decrease in neuronal density in these structures [Herculano-Houzel et al.: Proc Natl Acad Sci USA 2006;103:12138–12143]. Important remaining questions are whether such neuronal scaling rules within an order apply equally to all pertaining species, and whether they extend to closely related taxa. Here, we examine whether 4 other species of Rodentia, as well as the closely related rabbit (Lagomorpha), conform to the scaling rules identified previously for rodents. We report the updated neuronal scaling rules obtained for the average values of each species in a way that is directly comparable to the scaling rules that apply to primates [Gabi et al.: Brain Behav Evol 2010;76:32–44], and examine whether the scaling relationships are affected when phylogenetic relatedness in the dataset is accounted for. We have found that the brains of the spiny rat, squirrel, prairie dog and rabbit conform to the neuronal scaling rules that apply to the previous sample of rodents. The conformity to the previous rules of the new set of species, which includes the rabbit, suggests that the cellular scaling rules we have identified apply to rodents in general, and probably to Glires as a whole (rodents/lagomorphs), with one notable exception: the naked mole-rat brain is apparently an outlier, with only about half of the neurons expected from its brain size in its cerebral cortex and cerebellum.
Rodents; Brain size; Evolution; Neurons; Glia; Glires
The temporal cortex of grey squirrels contains three architectonically distinct regions. One of these regions, the temporal anterior (Ta) region has been identified in previous physiological and anatomical studies as containing several areas that are largely auditory in function. Consistent with this evidence, Ta has architectonic features that are internally somewhat variable, but overall sensory in nature. In contrast, the caudally adjoining temporal intermediate region (Ti) has architectonic features that suggest higher order and possibly multisensory processing. Finally, the most caudal region, composed of previously defined temporal medial (Tm) and temporal posterior (Tp) fields, again has more of the appearance of sensory cortex. To better understand their functional roles, we injected anatomical tracers into these regions to reveal their thalamic connections. As expected, the dorsal portion of Ta, containing two primary or primary-like auditory areas, received inputs from the ventral and magnocellular divisions of the auditory medial geniculate complex, MGv and MGm. The most caudal region, Tm plus Tp, received inputs from the large visual pulvinar of squirrels, possibly accounting for the sensory architectonic characteristics of this region. However, Tp additionally receives inputs from the magnocellular (MGm) and dorsal (MGd) divisions of the medial geniculate complex, implicating Tp in bisensory processing. Finally, the middle region, Ti, had auditory inputs from MGd and MGm, but not from the visual pulvinar, providing evidence that Ti has higher-order auditory functions. The results indicate that the architectonically distinct regions of temporal cortex of squirrels are also functionally distinct. Understanding how temporal cortex is functionally organized in squirrels can guide interpretations of temporal cortex organization in other rodents where architectonic subdivisions are not as obvious.
visual cortex; auditory cortex; multisensory cortex; lateral geniculate nucleus; pulvinar; rodents; medial geniculate; suprageniculate
Vesicular glutamate transporters (VGLUTs) control the storage and presynaptic release of glutamate in the central nervous system, and are involved in the majority of glutamatergic transmission in the brain. Two VGLUT isoforms, VGLUT1 and VGLUT2, are known to characterize complementary distributions of glutamatergic neurons in the rodent brain, which suggests that they are each responsible for unique circuits of excitatory transmission. In rodents, VGLUT2 is primarily utilized in thalamocortical circuits, and is strongly expressed in the primary sensory nuclei, including all areas of the visual thalamus. The distribution of VGLUT2 in the visual thalamus and midbrain has yet to be characterized in primate species. Thus, the present study describes the expression of VGLUT2 mRNA and protein across the visual thalamus and superior colliculus of prosimian galagos to provide a better understanding of glutamatergic transmission in the primate brain. VGLUT2 is strongly expressed in all six layers of the dorsal lateral geniculate nucleus, and much less so in the intralaminar zones, which correspond to retinal and superior collicular inputs, respectively. The parvocellular and magnocellular layers expressed VGLUT2 mRNA more densely than the koniocellular layers. A patchy distribution of VGLUT2 positive terminals in the pulvinar complex possibly reflects inputs from the superior colliculus. The upper superficial granular layers of the superior colliculus, with inputs from the retina, most densely expressed VGLUT2 protein, while the lower superficial granular layers, with projections to the pulvinar, most densely expressed VGLUT2 mRNA. The results are consistent with the conclusion that retinal and superior colliculus projections to the thalamus depend highly on the VGLUT2 transporter, as do cortical projections from the magnocellular and parvocellular layers of the lateral geniculate nucleus and neurons of the pulvinar complex.
lateral geniculate nucleus; superior colliculus; pulvinar; primate; glutamate
We examined the connections of posterior parietal cortex (PPC) with motor/premotor cortex (M1/PM) and other cortical areas. Electrical stimulation (500 ms trains) delivered to microelectrode sites evoked movements of reach, defense, and grasp, from distinct zones in M1/PM and PPC, in squirrel and owl monkeys. Tracer injections into M1/PM reach, defense, and grasp zones showed dense connections with M1/PM hand/forelimb representations. The densest inputs outside of frontal cortex were from PPC zones. M1 zones were additionally connected with somatosensory hand/forelimb representations in areas 3a, 3b, and 1 and the somatosensory areas of the upper bank of the lateral sulcus (S2/PV). Injections into PPC zones showed primarily local connections and the densest inputs outside of PPC originated from M1/PM zones. The PPC reach zone also received dense inputs from cortex caudal to PPC, which likely relayed visual information. In contrast, the PPC grasp zone was densely connected with the hand/forelimb representations of areas 3a, 3b, 1, and S2/PV. Thus, the dorsal parietal–frontal network involved in reaching was preferentially connected to visual cortex, whereas the more ventral network involved in grasping received somatosensory inputs. Additional weak interlinks between dissimilar zones (e.g., PPC reach and PPC grasp) were apparent and may coordinate actions.
intracortical electrical stimulation; motor cortex; parietal–frontal network; posterior parietal cortex; premotor cortex; reach and grasp
Connections of motor areas in the frontal cortex of prosimian galagos (Otolemur garnetti) were determined by injecting tracers into sites identified by microstimulation in the primary motor area (M1), dorsal premotor area (PMD), ventral premotor area (PMV), supplementary motor area (SMA), frontal eye field (FEF), and granular frontal cortex. Retrogradely labeled neurons for each injection were related to architectonically defined thalamic nuclei. Nissl, acetylcholinesterase, cytochrome oxidase, myelin, parvalbumin, calbindin, and Cat 301 preparations allowed the ventral anterior and ventral lateral thalamic regions, parvocellular and magnocellular subdivisions of ventral anterior nucleus, and anterior and posterior subdivisions of ventral lateral nucleus of monkeys to be identified. The results indicate that each cortical area receives inputs from several thalamic nuclei, but the proportions differ. M1 receives major inputs from the posterior subdivision of ventral lateral nucleus while premotor areas receive major inputs from anterior parts of ventral lateral nucleus (the anterior subdivision of ventral lateral nucleus and the anterior portion of posterior subdivision of ventral lateral nucleus). PMD and SMA have connections with more dorsal parts of the ventral lateral nucleus than PMV. The results suggest that galagos share many subdivisions of the motor thalamus and thalamocortical connection patterns with simian primates, while having less clearly differentiated subdivisions of the motor thalamus.
Motor Thalamus; Ventral Lateral Nucleus; Mediodorsal Nucleus; Supplementary Motor Area; Frontal Eye Field
The presynaptic storage and release of glutamate, an excitatory neurotransmitter, is modulated by a family of transport proteins known as vesicular glutamate transporters. Vesicular glutamate transporter 1 (VGLUT1) is widely distributed in the central nervous system of most mammalian and nonmammalian species, and regulates the uptake of glutamate into synaptic vesicles as well as the transport of filled glutamatergic vesicles to the terminal membrane during excitatory transmission. In rodents, VGLUT1 mRNA is primarily found in the neocortex, cerebellum, and hippocampus, and the VGLUT1 transport protein is involved in intercortical and corticothalamic projections that remain distinct from projections involving other VGLUT isoforms. With the exception of a few thalamic sensory nuclei, VGLUT1 mRNA is absent from subcortical areas and does not colocalize with other VGLUT mRNAs. VGLUT1 is similarly restricted to a few thalamic association nuclei and does not colocalize with other VGLUT proteins. However, recent work in primates has shown that VGLUT1 mRNA is also found in several subcortical nuclei as well as cortical areas, and that VGLUT1 may overlap with other VGLUT isoforms in glutamatergic projections. In order to expand current knowledge of VGLUT1 distributions in primates and gain insight on glutamatergic transmission in the visual system of primate species, we examined VGLUT1 mRNA and protein distributions in the lateral geniculate nucleus, pulvinar complex, superior colliculus, V1, V2, and the middle temporal area (MT) of prosimian galagos. We found that, similar to other studies in primates, VGLUT1 mRNA and protein are widely distributed in both subcortical and cortical areas. However, glutamatergic projections involving VGLUT1 are largely limited to intrinsic connections within subcortical and cortical areas, as well as the expected intercortical and corticothalamic projections. Additionally, VGLUT1 expression in galagos allowed us to identify laminar subdivisions of the superior colliculus, V1, V2, and MT.
excitatory neurotransmitter; vesicular glutamate transporters; glutamatergic projections; lateral geniculate nucleus; pulvinar complex; superior colliculus
The nodes of a parietal-frontal pathway that mediates grasping in primates are in anterior intraparietal area (AIP) and ventral premotor cortex (PMv). Nevertheless, multiple somatosensory and motor representations of the hand, respectively in parietal and frontal cortex, suggest that additional pathways remain unrealized. We explored this possibility in macaque monkeys by injecting retrograde tracers into grasp zones identified in M1, PMv, and area 2 with long train electrical stimulation. The M1 grasp zone was densely connected with other frontal cortex motor regions. The remainder of the connections originated from somatosensory areas 3a and S2/PV, and from the medial bank and fundus of the intraparietal sulcus (IPS). The PMv grasp zone was also densely connected with frontal cortex motor regions, albeit to a lesser extent than the M1 grasp zone. The remainder of the connections originated from areas S2/PV and aspects of the inferior parietal lobe such as PF, PFG, AIP, and the tip of the IPS. The area 2 grasp zone was densely connected with the hand representations of somatosensory areas 3b, 1, and S2/PV. The remainder of the connections was with areas 3a and 5 and the medial bank and fundus of the IPS. Connections with frontal cortex were relatively weak and concentrated in caudal M1. Thus, the three grasp zones may be nodes of parallel parietal-frontal pathways. Differential points of origin and termination of each pathway suggest varying functional specializations. Direct and indirect connections between those parietal-frontal pathways likely coordinate their respective functions into an accurate grasp.
Gorillas and orangutans are primates at least as large as humans, but their brains amount to about one third of the size of the human brain. This discrepancy has been used as evidence that the human brain is about 3 times larger than it should be for a primate species of its body size. In contrast to the view that the human brain is special in its size, we have suggested that it is the great apes that might have evolved bodies that are unusually large, on the basis of our recent finding that the cellular composition of the human brain matches that expected for a primate brain of its size, making the human brain a linearly scaled-up primate brain in its number of cells. To investigate whether the brain of great apes also conforms to the primate cellular scaling rules identified previously, we determine the numbers of neuronal and other cells that compose the orangutan and gorilla cerebella, use these numbers to calculate the size of the brain and of the cerebral cortex expected for these species, and show that these match the sizes described in the literature. Our results suggest that the brains of great apes also scale linearly in their numbers of neurons like other primate brains, including humans. The conformity of great apes and humans to the linear cellular scaling rules that apply to other primates that diverged earlier in primate evolution indicates that prehistoric Homo species as well as other hominins must have had brains that conformed to the same scaling rules, irrespective of their body size. We then used those scaling rules and published estimated brain volumes for various hominin species to predict the numbers of neurons that composed their brains. We predict that Homo heidelbergensis and Homo neanderthalensis had brains with approximately 80 billion neurons, within the range of variation found in modern Homo sapiens. We propose that while the cellular scaling rules that apply to the primate brain have remained stable in hominin evolution (since they apply to simians, great apes and modern humans alike), the Colobinae and Pongidae lineages favored marked increases in body size rather than brain size from the common ancestor with the Homo lineage, while the Homo lineage seems to have favored a large brain instead of a large body, possibly due to the metabolic limitations to having both.
Allometry; Brain size; Great apes; Human; Evolution, human; Neurons, number
The large size of primate brains is an impediment to obtaining high-resolution cell number maps of the cortex in humans and non-human primates. We present a rapid, flow cytometry-based cell counting method that can be used to estimate cell numbers from homogenized brain tissue samples comprising the entire cortical sheet. The new method, called the flow fractionator, is based on the isotropic fractionator (IF) method (Herculano-Houzel and Lent, 2005), but substitutes flow cytometry analysis for manual, microscope analysis using a Neubauer counting chamber. We show that our flow cytometry-based method for total cell estimation in homogenized brain tissue provides comparable data to that obtained using a counting chamber on a microscope. The advantages of the flow fractionator over existing methods are improved precision of cell number estimates and improved speed of analysis.
flow cytometry; Neubauer chamber; nuclear suspension; cell counting
A group of 5 genes, OCC1, testican-1, testican-2, 5-HT1B, and 5-HT2A, are selectively expressed in layer 4 (4C of Brodmann) of striate cortex (visual area V1) of both Old World macaques and New World marmoset monkeys. The expression of these genes is activity dependent, as expression is reduced after blocking retinal activity. Surprisingly, the pronounced expression pattern has not been found in rodents or carnivores. Thus, these genes may be highly expressed in V1 of some but perhaps not all primates. Here, we compared the gene expression in members of 3 major branches of primate evolution: prosimians, New World monkeys, and Old World monkeys. Although the expression pattern of 5-HT1B was well conserved, those of the other genes varied from the least distinct in prosimian galagos to successively more in New World owl monkeys, marmosets, squirrel monkeys, and Old World macaque monkeys. In owl monkeys, the expression of 5-HT2A was significantly reduced by monocular tetrodotoxin injection, while those of OCC1 and 5-HT1B were not. Thus, we propose that early primates had low levels of expression and higher levels emerged with anthropoid primates and became further enhanced in the Old World catarrhine monkeys that are more closely related to humans.
in situ hybridization; monocular inactivation; primate evolution; SPOCK; V1-specific
Posterior parietal cortex (PPC) links primate visual and motor systems and is central to visually guided action. Relating the anatomical connections of PPC to its neurophysiological functions may elucidate the organization of the parietal–frontal network. In owl and squirrel monkeys, long-duration electrical stimulation distinguished several functional zones within the PPC and motor/premotor cortex (M1/PM). Multijoint forelimb movements reminiscent of reach, defense, and grasp behaviors characterized each functional zone. In PPC, functional zones were organized parallel to the lateral sulcus. Thalamocortical connections of PPC and M1/PM zones were investigated with retrograde tracers. After several days of tracer transport, brains were processed, and labeled cells in thalamic nuclei were plotted. All PPC zones received dense inputs from the lateral posterior nucleus and the anterior pulvinar. PPC zones received additional projections from ventral lateral (VL) divisions of motor thalamus, which were also the primary source of input to M1/PM. Projections to PPC from rostral motor thalamus were sparse. Dense projections from ventral posterior (VP) nucleus of somatosensory thalamus distinguished the rostrolateral grasp zone from the other PPC zones. PPC connections with VL and VP provide links to cerebellar nuclei and the somatosensory system, respectively, that may integrate PPC functions with M1/PM.
intracortical microstimulation; motor cortex; premotor cortex; pulvinar; ventral lateral thalamus
What are the rules relating the size of the brain and its structures to the number of cells that compose them and their average sizes? We have shown previously that the cerebral cortex, cerebellum and the remaining brain structures increase in size as a linear function of their numbers of neurons and non-neuronal cells across 6 species of primates. Here we describe that the cellular composition of the same brain structures of 5 other primate species, as well as humans, conform to the scaling rules identified previously, and that the updated power functions for the extended sample are similar to those determined earlier. Accounting for phylogenetic relatedness in the combined dataset does not affect the scaling slopes that apply to the cerebral cortex and cerebellum, but alters the slope for the remaining brain structures to a value that is similar to that observed in rodents, which raises the possibility that the neuronal scaling rules for these structures are shared among rodents and primates. The conformity of the new set of primate species to the previous rules strongly suggests that the cellular scaling rules we have identified apply to primates in general, including humans, and not only to particular subgroups of primate species. In contrast, the allometric rules relating body and brain size are highly sensitive to the particular species sampled, suggesting that brain size is neither determined by body size nor together with it, but is rather only loosely correlated with body size.
Allometry; Brain size; Evolution; Glia, number; Neurons, number; Primates
The spinal cord can be considered a major sensorimotor interface between the body and the brain. How does the spinal cord scale with body and brain mass, and how are its numbers of neurons related to the number of neurons in the brain across species of different body and brain sizes? Here we determine the cellular composition of the spinal cord in eight primate species and find that its number of neurons varies as a linear function of cord length, and accompanies body mass raised to an exponent close to 1/3. This relationship suggests that the extension, mass and number of neurons that compose the spinal cord are related to body length, rather than to body mass or surface. Moreover, we show that although brain mass increases linearly with cord mass, the number of neurons in the brain increases with the number of neurons in the spinal cord raised to the power of 1.7. This faster addition of neurons to the brain than to the spinal cord is consistent with current views on how larger brains add complexity to the processing of environmental and somatic information.
Allometry; Number of neurons; Evolution; Connectivity
Despite the lack of ipsilateral receptive fields (RFs) for neurons in the hand representation of area 3b of primary somatosensory cortex, interhemispheric interactions have been reported to varying degrees. We investigated spatiotemporal properties of these interactions to determine: response types; timing between stimuli to evoke the strongest bimanual interactions; topographical distribution of effects; and their dependence on similarity of stimulus locations on the two hands. We analyzed response magnitudes and latencies of single neurons and multi-neuron clusters recorded from 100-electrode arrays implanted in one hemisphere of each of two anesthetized owl monkeys. Skin indentations were delivered to the two hands simultaneously and asynchronously at mirror locations (matched sites on each hand) and non-mirror locations. Since multiple neurons were recorded simultaneously, stimuli on the contralateral hand could be within or outside of the classical RFs of any given neuron. For most neurons, stimulation on the ipsilateral hand suppressed responses to stimuli on the contralateral hand. Maximum suppression occurred when the ipsilateral stimulus was presented 100ms before the contralateral stimulus onset (P < 0.0005). The longest stimulus onset delay tested (500ms) allowed contralateral responses to recover to control levels (P = 0.428). Stimulation on mirror digits did not differ from stimulation on non-mirror locations (P = 1.000). These results indicate that interhemispheric interactions are common in area 3b, somewhat topographically diffuse, and maximal when the suppressing ipsilateral stimulus preceded the contralateral stimulus. Our findings point to a neurophysiological basis for “interference” effects found in human psychophysical studies of bimanual stimulation.
area 3b; bimanual; interhemispheric; multielectrode; primate; Utah array