João G. Franca

Parallel Evolution of Cortical Areas Involved in Skilled Hand Use

Dexterous hands, used to manipulate food, tools, and other objects, are one of the hallmarks of primate evolution. However, the neural substrate of fine manual control necessary for these behaviors remains unclear. Here, we describe the functional organization of parietal cortical areas 2 and 5 in the cebus monkey. Whereas other New World monkeys can be quite dexterous, and possess a poorly developed area 5, cebus monkeys are the only New World primate known to use a precision grip, and thus have an extended repertoire of manual behaviors. Unlike other New World Monkeys, but much like the macaque monkey, cebus monkeys possess a proprioceptive cortical area 2 and a well developed area 5, which is associated with motor planning and the generation of internal body coordinates necessary for visually guided reaching, grasping, and manipulation. The similarity of these fields in cebus monkeys and distantly related macaque monkeys with similar manual abilities indicates that the range of cortical organizations that can emerge in primates is constrained, and those that emerge are the result of highly conserved developmental mechanisms that shape the boundaries and topographic organizations of cortical areas.

VISUAL RESPONSE PROPERTIES OF PRETECTAL UNITS IN THE NUCLEUS OF THE OPTIC TRACT OF THE OPOSSUM

SummarySingle-units were recorded from the nucleus of the optic tract. Most of the units showed excitation in response to random check patterns presented on a tangent screen to the contralateral eye, moving in a temporal to nasal direction and/or inhibition in the opposite direction. The excitatory response to the temporal to nasal movement, observed in most units, was unchanged throughout the range of speeds tested, except for a decrease at the slowest (0.6 deg/s) and fastest (150 deg/s) speeds. On the other hand, the inhibitory responses evoked by a nasal to temporal movement, had a peak between 3 and 16 deg/s which decreased towards both extremes. An average of 45% of the units were influenced by the stimulation of the ipsilateral eye. In one third of them the response was very weak. In the remainder, the mean frequency of spikes in one direction of the horizontal movement was more than twice that in the opposite stimulus direction. In the great majority of these units, stimulation of each eye yielded the same overall pattern of directionality, that is, movement of the stimulus towards the recording side led to excitation and/or movement in the reverse direction led to inhibition. Inhibition was stronger than excitation in most ipsilaterally responding units. Excitatory responses elicited by the ipsilateral eye were always weaker than those by the contralateral but in a few cases the ipsilateral inhibitory component was more prominent than the contralateral one.

The organization of somatosensory cortex in the short-tailed opossum ( Monodelphis domestica )

The organization of neocortex in the short-tailed opossum ( Monodelphis domestica ) was explored with multiunit microelectrode recordings from middle layers of cortex. Microelectrode maps were subsequently related to the chemoarchitecture of flattened cortical preparations, sectioned parallel to the cortical surface and processed for either cytochrome oxidase (CO) or NADPH-diaphorase (NADPHd) histochemistry. The recordings revealed the presence of at least two systematic representations of the contralateral body surface located in a continuous strip of cortex running from the rhinal sulcus to the medial wall. The primary somatosensory area (S1) was located medially while secondary somatosensory cortex (S2) formed a laterally located mirror image of S1. Auditory cortex was located in lateral cortex at the caudal border of S2, and some electrode penetrations in this area responded to both auditory and somatosensory stimulation. Auditory cortex was outlined by a dark oval visible in flattened brain sections. A large primary visual cortex (V1) was located at the caudal pole of cortex, and also consistently corresponded to a large chemoarchitecturally visible oval. Cortex just rostral and lateral to V1 responded to visual stimulation, while bimodal auditory/visual responses were obtained in an area between V1 and somatosensory cortex. The results are compared with brain organization in other marsupials and with placentals and the evolution of cortical areas in mammals is discussed.The organization of neocortex in the short-tailed opossum (Monodelphis domestica) was explored with multiunit microelectrode recordings from middle layers of cortex. Microelectrode maps were subsequently related to the chemoarchitecture of flattened cortical preparations, sectioned parallel to the cortical surface and processed for either cytochrome oxidase (CO) or NADPH-diaphorase (NADPHd) histochemistry. The recordings revealed the presence of at least two systematic representations of the contralateral body surface located in a continuous strip of cortex running from the rhinal sulcus to the medial wall. The primary somatosensory area (S1) was located medially while secondary somatosensory cortex (S2) formed a laterally located mirror image of S1. Auditory cortex was located in lateral cortex at the caudal border of S2, and some electrode penetrations in this area responded to both auditory and somatosensory stimulation. Auditory cortex was outlined by a dark oval visible in flattened brain sections. A large primary visual cortex (V1) was located at the caudal pole of cortex, and also consistently corresponded to a large chemoarchitecturally visible oval. Cortex just rostral and lateral to V1 responded to visual stimulation, while bimodal auditory/visual responses were obtained in an area between V1 and somatosensory cortex. The results are compared with brain organization in other marsupials and with placentals and the evolution of cortical areas in mammals is discussed.

Callosal Axon Arbors in the Limb Representations of the Somatosensory Cortex (SI) in the Agouti (Dasyprocta primnolopha)

The present report compares the morphology of callosal axon arbors projecting from and to the hind‐ or forelimb representations in the primary somatosensory cortex (SI) of the agouti (Dasyprocta primnolopha), a large, lisencephlic Brazilian rodent that uses forelimb coordination for feeding. Callosal axons were labeled after single pressure (n = 6) or iontophoretic injections (n = 2) of the neuronal tracer biotinylated dextran amine (BDA, 10 kD), either into the hind‐ (n = 4) or forelimb (n = 4) representations of SI, as identified by electrophysiological recording. Sixty‐nine labeled axon fragments located across all layers of contralateral SI representations of the hindlimb (n = 35) and forelimb (n = 34) were analyzed. Quantitative morphometric features such as densities of branching points and boutons, segments length, branching angles, and terminal field areas were measured. Cluster analysis of these values revealed the existence of two types of axon terminals: Type I (46.4%), less branched and more widespread, and Type II (53.6%), more branched and compact. Both axon types were asymmetrically distributed; Type I axonal fragments being more frequent in hindlimb (71.9%) vs. forelimb (28.13%) representation, while most of Type II axonal arbors were found in the forelimb representation (67.56%). We concluded that the sets of callosal axon connecting fore‐ and hindlimb regions in SI are morphometrically distinct from each other. As callosal projections in somatosensory and motor cortices seem to be essential for bimanual interaction, we suggest that the morphological specialization of callosal axons in SI of the agouti may be correlated with this particular function. J. Comp. Neurol. 500:255–266, 2007.

The barrel field of the adult mouse sml cortex as revealed by NADPH-diaphorase histochemistry

The main goal of the present work was to investigate the pattern of NADPH-diaphorase activity in the somatosensory cortex of the adult mouse. Our results show that this enzyme, which is responsible for the production of the neuronal messenger nitric oxide, is abundant within the neuropil of Sml cortex, revealing the complete pattern of barrel fields. A previous study, however, had reported that NADPH-diaphorase reactivity within the barrels was transient, disappearing after the second postnatal week. We hypothesize that the massive occurrence of NADPH-diaphorase in the barrel fields of the adult mouse brain is related to the potential for plastic changes in the somatosensory cortex that is maintained throughout maturity.

Neuropil reactivity, distribution and morphology of NADPH diaphorase type I neurons in the barrel cortex of the adult mouse

The mouse, like a few other rodent and marsupial species, displays a striking modular architecture in its primary somatosensory cortex (SI). These modules, known as barrels, are mostly defined by the peculiar arrangement of granule cells and thalamic axons in layer IV. In the present work, we studied both the distribution and morphology of neurons stained for NADPH diaphorase (NADPH-d) and neuropil reactivity in the posteromedial barrel subfield (PMBSF), which represents the mystacial whiskers. We then compared our results with previous descriptions of NADPH-d distribution in both neonatal and young mice. We found two types of neurons in the PMBSF: type I neurons, which have large cell bodies and are heavily stained by the NADPH-d reaction; and type II neurons, characterized by relatively small and poorly stained cell bodies. The distribution of type I cells in the PMBSF was not homogenous, with cells tending to concentrate in septa between barrels. Moreover, the cells found in septal region possess both a larger and more complex dendritic arborization than cells located inside barrels. Our findings are at variance with results from other groups that reported both an absence of type II cells and a homogeneous distribution of type I cells in the PMBSF of young animals. In addition, our results show a distribution of type I cells which is very similar to that previously described for the rats barrel field.

A morphometric study of the progressive changes on NADPH diaphorase activity in the developing rat’s barrel field

The distribution of NADPH diaphorase (NADPH-d)/nitric oxide synthase (NOS) neurons was evaluated during the postnatal development of the primary somatosensory cortex (SI) of the rat. Both cell counts and area measurements of barrel fields were carried out throughout cortical maturation. In addition, NADPH-d and cytochrome oxidase (CO) activities were also compared in both coronal and tangential sections of rat SI between postnatal days (P) 10 and 90. Throughout this period, the neuropil distributions of both enzymes presented a remarkable similarity and have not changed noticeably. Their distribution pattern show the PMBSF as a two-compartmented structure, displaying a highly reactive region (barrel hollows) flanked by less reactive regions (barrel septa). The number of NADPH-d neurons increased significantly in the barrel fields between P10 and P23, with peak at P23. The dendritic arborization of NADPH-d neurons became more elaborated during barrel development. In all ages evaluated, the number of NADPH-d cells was always higher in septa than in the barrel hollows. Both high neuropil reactivity and differential distribution of NADPH-d neurons during SI development suggest a role for nitric oxide throughout barrel field maturation.

A connection to the past: Monodelphis domestica provides insight into the organization and connectivity of the brains of early mammals

The current experiment is one of a series of comparative studies in our laboratory designed to determine the network of somatosensory areas that are present in the neocortex of the mammalian common ancestor. Such knowledge is critical for appreciating the basic functional circuitry that all mammals possess and how this circuitry was modified to generate species‐specific, sensory‐mediated behavior. Our animal model, the gray short‐tailed opossum (Monodelphis domestica), is a marsupial that is proposed to represent this ancestral state more closely than most other marsupials and, to some extent, even monotremes. We injected neuroanatomical tracers into the primary somatosensory area (S1), rostral and caudal somatosensory fields (SR and SC, respectively), and multimodal cortex (MM) and determined their connections with other architectonically defined cortical fields. Our results show that S1 has dense intrinsic connections, dense projections from the frontal myelinated area (FM), and moderate projections from S2 and SC. SR has strong projections from several areas, including S1, SR, FM, and piriform cortex. SC has dense projections from S1, moderate to strong projections from other somatosensory areas, FM, along with connectivity from the primary (V1) and second visual areas. Finally, MM had dense intrinsic connections, dense projections from SC and V1, and moderate projections from S1. These data support the proposition that ancestral mammals likely had at least four specifically interconnected somatosensory areas, along with at least one multimodal area. We discuss the possibility that these additional somatosensory areas (SC and SR) are homologous to somatosensory areas in eutherian mammals. J. Comp. Neurol. 521:3877–3897, 2013.

The brain decade in debate: VI. Sensory and motor maps: dynamics and plasticity

This article is an edited transcription of a virtual symposium promoted by the Brazilian Society of Neuroscience and Behavior (SBNeC). Although the dynamics of sensory and motor representations have been one of the most studied features of the central nervous system, the actual mechanisms of brain plasticity that underlie the dynamic nature of sensory and motor maps are not entirely unraveled. Our discussion began with the notion that the processing of sensory information depends on many different cortical areas. Some of them are arranged topographically and others have non-topographic (analytical) properties. Besides a sensory component, every cortical area has an efferent output that can be mapped and can influence motor behavior. Although new behaviors might be related to modifications of the sensory or motor representations in a given cortical area, they can also be the result of the acquired ability to make new associations between specific sensory cues and certain movements, a type of learning known as conditioning motor learning. Many types of learning are directly related to the emotional or cognitive context in which a new behavior is acquired. This has been demonstrated by paradigms in which the receptive field properties of cortical neurons are modified when an animal is engaged in a given discrimination task or when a triggering feature is paired with an aversive stimulus. The role of the cholinergic input from the nucleus basalis to the neocortex was also highlighted as one important component of the circuits responsible for the context-dependent changes that can be induced in cortical maps.

Morphometric variability of nicotinamide adenine dinucleotide phosphate diaphorase neurons in the primary sensory areas of the rat.

Even though there is great regional variation in the distribution of inhibitory neurons in the mammalian isocortex, relatively little is known about their morphological differences across areal borders. To obtain a better understanding of particularities of inhibitory circuits in cortical areas that correspond to different sensory modalities, we investigated the morphometric differences of a subset of inhibitory neurons reactive to the enzyme nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) within the primary auditory (A1), somatosensory (S1), and visual (V1) areas of the rat. One hundred and twenty NADPH-d-reactive neurons from cortical layer IV (40 cells in each cortical area) were reconstructed using the Neurolucida system. We collected morphometric data on cell body area, dendritic field area, number of dendrites per branching order, total dendritic length, dendritic complexity (Sholl analysis), and fractal dimension. To characterize different cell groups based on morphology, we performed a cluster analysis based on the previously mentioned parameters and searched for correlations among these variables. Morphometric analysis of NADPH-d neurons allowed us to distinguish three groups of cells, corresponding to the three analyzed areas. S1 neurons have a higher morphological complexity than those found in both A1 and V1. The difference among these groups, based on cluster analysis, was mainly related to the size and complexity of dendritic branching. A principal component analysis (PCA) applied to the data showed that area of dendritic field and fractal dimension are the parameters mostly responsible for dataset variance among the three areas. Our results suggest that the nitrergic cortical circuitry of primary sensory areas of the rat is differentially specialized, probably reflecting peculiarities of both habit and behavior of the species.