Organizing principles of cortical integration in the rat neostriatum: Corticostriate map of the body surface is an ordered lattice of curved laminae and radial points

Abstract

The neuroanatomic organizing principles underlying integrative functions in the striatum are only partially understood. Within the three major subdivisions of the striatum-sensorimotor, associative, and limbic--longitudinal zones of axonal plexuses from the cerebral cortex end in bands and clusters that innervate cell groups. To identify organizing principles of the corticostriate bands and clusters, we localized somatosensory cortical cells receptive to light touch on the hindlimb, forelimb, or vibrissae by extracellular recording, and we labeled their projections by iontophoretic application of dextran anterograde tracers. The results show that cortical cells in columnar groups project to the striatum in the form of successive strips, or laminae, that parallel the curve of the external capsule. The vibrissae somatosensory cortex projects to the most lateral lamina. Just medial to the vibrissae projection, the major axonal arborizations arising from hindlimb and forelimb somatosensory cortex are organized within a common lamina, where they interdigitate and overlap as well as remain separate. In addition, the hindlimb and forelimb cortex send small projections to the vibrissae lamina, and vice versa, forming broken, radially oriented lines of points across the laminar strips. The major somatosensory projections are in the dorsolateral, calbindin-poor sensorimotor striatum, whereas the radially oriented projection points extend into the medial, calbindin-rich associative striatum. Extending previous studies of corticostriate projections, this report shows a grid translation of columnar somatosensory cortical inputs into striatum and a detailed map for the rat sensorimotor zone. The lattice-like grid is a novel functional/neuroanatomic organization that is ideal for distributing, combining, and integrating information for sensorimotor and cognitive processing.

Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats

“…Finally, the small size of the IT-type terminals and the diffuse nature of the IT projection to striatum may require synchrony of firing from diverse cortical areas for IT input to activate striato-EP-SNr neurons (Wilson, 1992). This is consistent with the presumed role of direct pathway neurons in promoting movement based on integration of diverse cortical input and with evidence for convergent projections from related cortical areas to individual striatal domains (Flaherty and Graybiel, 1991;Brown et al, 1998;Hoffer and Alloway, 2001). …”

The effects of cocaine: A shifting target over the course of addiction

“…This hierarchical arrangement, perhaps, underlies the manner in which the pattern of afferents to the striatum determines the functional response to cocaine, and explains how this response expands with increasing durations of exposure. In addition, functional activity in the striatum is also directly influenced by input from the cortex (Brown et al, 1998). Reciprocal and nonreciprocal cortico-thalamic connections may further amplify the impact of cocaine on the cortex, and in turn the striatal circuits to which these areas project.…”

The Reward Circuit: Linking Primate Anatomy and Human Imaging

“…Overall, there appears to be a dual organization that permits both parallel and integrative processing. Thus, the ventral cortico-basal ganglia network, while at the heart of reward processing, does not work in isolation (Belin and Everitt, 2008;Bevan et al, 1997;Brown et al, 1998;Draganski et al, 2008;Haber et al, 2000Haber et al, , 2006Joel and Weiner, 1994;Kasanetz et . Schematic illustrating key structures and pathways of the reward circuit.…”