The neocortex has a remarkable capacity to alter its functional organization and connectivity in response to sensory loss, particularly if this loss occurs early in life. A key question is whether this cross-modal reorganization is driven by sensory deprivation or by enhanced use of the spared senses. We investigated how different rearing environments shape neural responses in primary somatosensory cortex (S1) of short-tailed opossums (Monodelphis domestica), following elimination of visual inputs through bilateral enucleation in early development. Early blind and sighted littermates of either sex were reared in enriched environments to promote active tactile exploration in three-dimensional space or in standard laboratory cages. In adulthood, both enriched groups showed adaptive changes in exploration patterns and gap crossing behaviors relative to standard-reared counterparts. Thus, early blind animals showed behavioral compensation when challenged by complex environments. Enriched rearing increased selectivity of S1 neural responses to whisker touch and altered receptive field shapes such that they were less horizontally anisotropic. This shift was strongest in enriched early blind animals, enhancing tuning along the behaviorally relevant horizontal axis more than in standard-reared early blind animals. Thus, alterations in receptive fields of neurons in S1 following early blindness were amplified by environmental complexity. Sighted opossums reared with enrichment also showed similar whisker receptive field plasticity, though to a slightly lower degree. These results demonstrate that the rearing environment strongly influences the reorganization of cortex that processes inputs from the spared senses, underscoring the role of experience in directing compensatory plasticity following early sensory loss.

In the following review, we describe the types of phenotypic changes to the neocortex that occur over the longer time scale of evolution, and over the shorter time scale of an individual lifetime. To understand how phenotypic variability emerges in the neocortex, it is important to consider the cortex as part of an integrated system of the brain, the body, the environment in which the brain and body develops and evolves, and the affordances available within a particular environmental context; changes in any part of this brain/body/environment network impact the neocortex. We provide data from comparative studies on a wide variety of mammals that demonstrate that body morphology, the sensory epithelium, and the use of a particular morphological structure have a profound impact on neocortical organization and connections. We then discuss the genetic and epigenetic factors that contribute to the development of the neocortex, as well as the role of spontaneous and sensory driven activity in constructing a nervous system. Although the evolution of the neocortex cannot be studied directly, studies in which developmental processes are experimentally manipulated provide important insights into how phenotypic transformations could occur over the course of evolution and demonstrate that relatively small alterations to the body and/or the environment in which an individual develops can manifest as large changes to the neocortex. Finally, we discuss how these phenotypic alterations to the neocortex impact an important target of selection – behavior.

Advances in sequencing techniques have made comparative studies of gene expression a current focus for understanding evolutionary and developmental processes. However, insights into the spatial expression of genes have been limited by a lack of robust methodology. To overcome this obstacle, we developed methods and software tools for quantifying and comparing tissue-wide spatial patterns of gene expression within and between species. Here, we compare cortex-wide expression of RZRβ and Id2 mRNA across early postnatal development in mice and voles. We show that patterns of RZRβ expression in neocortical layer 4 are highly conserved between species but develop rapidly in voles and much more gradually in mice, who show a marked expansion in the relative size of the putative primary visual area across the first postnatal week. Patterns of Id2 expression, by contrast, emerge in a dynamic and layer-specific sequence that is consistent between the two species. We suggest that these differences in the development of neocortical patterning reflect the independent evolution of brains, bodies, and sensory systems in the 35 million years since their last common ancestor.

Bats have evolved behavioral specializations that are unique among mammals, including self-propelled flight and echolocation. However, areas of motor cortex that are critical in the generation and fine control of these unique behaviors have never been fully characterized in any bat species, despite the fact that bats compose similar to 25% of extant mammalian species. Using intracortical microstimulation, we examined the organization of motor cortex in Egyptian fruit bats (Rousettus aegyptiacus), a species that has evolved a novel form of tongue-based echolocation.(1,2) We found that movement representations include an enlarged tongue region containing discrete subregions devoted to generating distinct tongue movement types, consistent with their behavioral specialization generating active sonar using tongue clicks. This magnification of the tongue in motor cortex is comparable to the enlargement of somatosensory representations in species with sensory specializations.(3-5) We also found a novel degree of coactivation between the forelimbs and hindlimbs, both of which are involved in altering the shape and tension of wing membranes during flight. Together, these findings suggest that the organization of motor cortex has coevolved with peripheral morphology in bats to support the unique motor demands of flight and echolocation.

This protocol presents a workflow for detecting differences in kinematics between experimental conditions. It is tailored for short-tailed opossums but can be applied to any species capable of completing the ladder rung task. There are four phases of this protocol: (1) data collection, (2) pose tracking, (3) analysis of single trials, and (4) cross-condition comparisons. This pipeline implements aspects of machine learning and signal processing, allowing for rapid data analysis that provides insight into how animals perform this task.For complete details on the use and execution of this protocol, please refer to Englund et al. (2020).

Advances in sequencing techniques have made comparative studies of gene expression a current focus for understanding evolutionary and developmental processes. However, insights into the spatial expression of genes have been limited by a lack of robust methodology. We therefore developed a set of algorithms for quantifying and comparing tissue-wide spatial patterns of gene expression within and across species. Here we apply these algorithms to compare cortex-wide expression of Id2 and RZRβ mRNA in early postnatal mice and voles. We show that neocortical patterns of Id2 expression are moderately conserved between species, but that the degree of conservation varies by cortical layer and area. By comparison, patterns of RZRβ expression are highly conserved in somatosensory areas, and more variable between species in visual and auditory areas. We consider if these differences reflect independent evolution in the 35 million years since the last common ancestor.

ABSTRACT The early loss of vision results in a reorganized visual cortex that processes tactile and auditory inputs. Recent studies in the short-tailed opossum ( Monodelphis domestica) found that the connections and response properties of neurons in somatosensory cortex of early blind animals are also altered. While research in humans and other mammals shows that early vision loss leads to heightened abilities on discrimination tasks involving the spared senses, if and how this superior discrimination leads to adaptive sensorimotor behavior has yet to be determined. Moreover, little is known about the extent to which blind animals rely on the spared senses. Here, we tested early blind opossums on a sensorimotor task involving somatosensation and found that they had increased limb placement accuracy. However, increased reliance on tactile inputs in early blind animals resulted in greater deficits in limb placement and behavioral flexibility when the whiskers were trimmed.

The early loss of vision results in a reorganized neocortex, affecting areas of the brain that process both the spared and lost senses, and leads to heightened abilities on discrimination tasks involving the spared senses. Here, we used performance measures and machine learning algorithms that quantify behavioral strategy to determine if and how early vision loss alters adaptive sensorimotor behavior. We tested opossums on a motor task involving somatosensation and found that early blind animals had increased limb placement accuracy compared with sighted controls, while showing similarities in crossing strategy. However, increased reliance on tactile inputs in early blind animals resulted in greater deficits in limb placement and behavioral flexibility when the whiskers were trimmed. These data show that compensatory cross-modal plasticity extends beyond sensory discrimination tasks to motor tasks involving the spared senses and highlights the importance of whiskers in guiding forelimb control.

Which areas of the neocortex are involved in the control of movement, and how is motor cortex organized across species? Recent studies using long-train intracortical microstimulation demonstrate that in addition to M1, movements can be elicited from somatosensory regions in multiple species. In the rat, M1 hindlimb and forelimb movement representations have long been thought to overlap with somatosensory representations of the hindlimb and forelimb in S1, forming a partial sensorimotor amalgam. Here we use long-train intracortical microstimulation to characterize the movements elicited across frontal and parietal cortex. We found that movements of the hindlimb, forelimb, and face can be elicited from both M1 and histologically defined S1 and that representations of limb movement types are different in these two areas. Stimulation of S1 generates retraction of the contralateral forelimb, while stimulation of M1 evokes forelimb elevation movements that are often bilateral, including a rostral region of digit grasping. Hindlimb movement representations include distinct regions of hip flexion and hindlimb retraction evoked from S1 and hip extension evoked from M1. Our data indicate that both S1 and M1 are involved in the generation of movement types exhibited during natural behavior. We draw on these results to reconsider how sensorimotor cortex evolved.

In this paper, our goal is to explore what is known about the role of social touch during development. We first address the neural substrates of social touch and the role of tactile experience in neural development. We discuss natural variation in early exposure to social touch, followed by a discussion on experimental manipulations of social touch during development and “natural experiments”, such as early institutionalization. We then consider the role of other developmental and experiential variables that predict social touch in adults. Throughout, we propose and consider new theoretical models of the role of social touch during development on later behavior and neurobiology.