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

Abstract

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 cortex (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 cortex 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 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°, 2°and 3°branches of apical and 1°and 2°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 targe...

Processing Afferent Proprioceptive Information at the Main Cuneate Nucleus of Anesthetized Cats

“…Area 3a is part of a network involved in proprioception, postural control, and the generation of coordinated movements. It receives proprioceptive input (reviewed by Jones and Porter, 1980) and sends descending fibers that might affect mvCN neurons through different routes, including direct corticobulbar fibers and collaterals of corticospinal axons (Lamas et al, 1994;Martinez et al, 1995), and via area 2 and motor cortex (Porter, 1997). Various options are possible to explain our data: (1) Cortico-mvCN fibers from area 3a have slower conduction speeds than those from the motor cortex; experimental evidence for this is lacking.…”

“…Corticobulbar fibers are slower conducting than corticospinal fibers (Lamas et al, 1994). (3) Stimulation of area 3a indirectly affects mvCN neurons through the motor cortex either directly (Zarzecki et al, 1978;Asanuma et al, 1982) or after a previous relay in area 2 (Porter, 1997).…”

Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study

“…Because the proximal dendrites in BA3-1-2 are essential to the intrinsic corticocortical connections of this region [Porter, 1997], these pyramidal neurons appear to mature relatively quickly and are likely crucial to the relatively early functional maturity of BA3-1-2 [Chugani et al, 1987]. Although visual cortical regions may mature somewhat later than BA3-1-2 in terms of sulcal-gyral development [Ruoss et al, 2001], visual cortex nevertheless matures earlier ontogenetically than does the overall brain in terms of laminar development, functional ability, synaptogenesis, and local metabolic rates [Sauer et al, 1983;Chugani and Phelps, 1986;Huttenlocher, 1990].…”

Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row

“…In primates, for example, Brodmann cortical areas 3a, 1, and 2 project directly to cortical area 4, presumably to transmit both proprioceptive and cutaneous information (Vogt and Pandya, 1977;Jones et al, 1978;Strick and Preston, 1982;Ghosh et al, 1987;Huerta and Pons, 1990;Stepniewska et al, 1993;Burton and Fabri, 1995). Direct projections from SI to MI have also been demonstrated in cats and rodents (Asanuma et al, 1982;Donoghue and Parham, 1983;Porter and Sakamoto, 1988;Fabri and Burton, 1991;Miyashita et al, 1994;Izraeli and Porter, 1995;Porter, 1997). Furthermore, several electrophysiology studies indicate that direct projections from SI to MI are capable of modulating neuronal responses in MI (Herman et al, 1985;Kosar et al, 1985;Zarzecki, 1986;Kaneko et al, 1994;Farkas et al, 1999;Kelly et al, 2001).…”