Morphological Characterization of a Cortico-cortical relay in the cat sensorimotor cortex.

One feature of the cerebral cortex circuitry is the complex network of fibers which links its different functional regions. Our knowledge of the specific relationships between neurons which form these pathways is limited. The cortico-cortical connections between primary somatosensory cortex (SI) and primary motor cortext (MI) were the focus of the study. The aims were twofold: first, to identify characteristics of inter-areal cortico-cortical connections; and second, to determine if pathways exist which support the notion that peripheral signals are integrated in the somatosensory cortext before being relayed to the motor cortex. Neurons in area 2 of SI, which projected to the motor cortex were identified. The morphological characteristics of these neurons and the pattern of input that they received from the area 3a were determined. The fluorescent retrograde tracer, fast blue, was injected into the electrophysiologically defined forepaw representation of motor cortex and the anterograde tracer, dextran-tetramethylrhodamine (DR), was injected into the somatotopically matched region of area 3a. Labeled neurons in area 2 which were located in a field of labeled axons arising from area 3a were identified in fixed tissue sections. Some of these labeled cells were impaled with a Lucifer yellow (LY)-filled micropipette and were intracellulary labeled by iontophoretic injection of LY Cells in area 2 that projected to the motor cortex were located primarily in layers II-III. They were all classified as pyramidal neurons and were morphologically similar. Their apical dendrites for the most part did not extend beyond layer II. Their apical tufts exhibited 2-4 branches within layers II-III, while basal dendrites exhibited more numerous tertiary basal dendritic branches. Light microscopic (LM) examination revealed the presence of appositions between LY-filled profiles and DR-labeled axons. Appositions were observed between swellings along DR-labeled axons and dendritic shafts or spines of 1 degrees, 2 degrees and 3 degrees branches of apical and 1 degrees and 2 degrees branches of basal dendrites. The appositions were primarily on proximal segments of labeled dendritic shafts. Fewer appositions with distal dendrites were observed and some of these were with dendritic spines. No appositions with the somata were observed. Only one or two appositions were observed for individual cells. The pattern of cortico-cortical synaptic input arising from area 3a onto this population of cells was predicted from these LM findings. An ultrastructural analysis was performed to confirm the existence of contacts and the predicted pattern of connectivity. Neurons in area 2 which projected to the motor cortex, and area 3a axons which projected to area 2, were identified with electron dense retrograde and anterograde tracers respectively. Labeled neurons located in a field of labeled axons were examined throughout a sequential series of ultrathin sections. Electron microscopic analysis revealed a similar pattern, but with a slightly higher density of synaptic input (1-8 contacts per target cell) than that predicted from the LM studies. These results revealed a specific density and pattern of coritco-cortical input onto an identified population of cortico-cortical projection neurons. Individual target cells received only sparse input from a functionally different but somatotopically related region of the cortex. The pattern of input onto cells was unexpected in that most axons contacted the shafts of proximal dendrites. This aspect of the connection may exemplify a unique feature of the cortical circuit which helps to define its functional role. The significance of these results in defining cortical function is that the particular cortical circuit described may provide an anatomical substrate for the modulation of motor cortex activity by integrated signals from the sensory cortex. The synaptic relationships of neurons in this pathway may be characteristic of i