Cellular physiology of the turtle visual cortex: distinctive properties of pyramidal and stellate neurons

Abstract

The electrophysiological properties of neurons in the three-layered dorsal cortex of the turtle, Pseudemys scripta elegans, have been studied in vitro. Intracellular recordings suggested two distinct classes of neuronal behavior. Cell labeling with either Lucifer Yellow or horseradish peroxidase revealed that these behaviors correlated with the two morphological classes of cortical neurons: pyramidal cells and stellate cells. Examination of Golgi-stained neurons of dorsal cortex did not uncover any other obvious classes. Pyramidal cells had their somata in the cell layer, and extended several densely spined apical dendrites through the molecular layer to the pia. They also had spiny basilar dendrites directed through the subcellular layer toward the ependymal border. Physiologically, pyramidal cells had relatively prolonged action potentials that showed marked frequency adaptation during a sustained suprathreshold current pulse. Their most striking characteristic was a tendency to fire two discrete sizes of action potential, one small (mean = 34 mV) and of relatively low threshold, the other large (mean = 76 mV) and of higher threshold. We hypothesize that at least some small spikes arise from distal dendritic sites, whereas large spikes are somatically generated. Both spikes were tetrodotoxin-sensitive, although calcium-dependent electrogenesis occurred when potassium channels were blocked. In contrast to pyramidal cells, the somata of stellate cells were found in the molecular and subcellular zones. Their dendrites tended to be horizontally oriented and spine-free. Stellate cells had relatively brief action potentials, each of which was followed by a large but short-lasting undershoot of membrane potential. Stellate cells showed little or no spike frequency adaptation. Spike amplitudes were always relatively uniform and large (mean = 73 mV). Thus, in the dorsal cortex of turtles, the pyramidal cells, which are projection neurons, and stellate cells, which are local GABAergic inhibitory neurons, have distinctly different membrane characteristics. The physiological properties of the two types of turtle cortical neurons are very similar to their counterparts in cortical structures of the mammalian telencephalon.

Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology

“…The pronounced decrease in firing frequency over time in response to a constant current pulse (spike frequency adaptation) appears to be a ubiquitous property of pyramidal cells (e.g., Koike et al, 1970;Lanthorn et al, 1984;Stafstrom et al, 1984a;McCormick et al, 1985;Connors and Kriegstein, 1986;Connors et al, 1988). Usually, most of the adaptation occurs during the first few interspike intervals, as was the case in the present study.…”

Neurotransmitter organization and connections of turtle cortex: implications for the evolution of mammalian isocortex

“…Two basic types of neurons are found in turtle dorsal cortex, pyramidal and nonpyramidal (Smith et al, 1980;Connors and Kriegstein, 1986). The pyramidal neurons, which are located in the cellular layer, possess dendrites that branch widely and extend out toward the pial surface.…”

“…3). The pyramidal neurons appear to be the main input and output neurons of turtle cortex, while the nonpyramidal neurons appear to be involved in local circuit interactions (Smith et al, 1980;Connors and Kriegstein, 1986). Anatomical studies have shown that thalamic inputs terminate on the dendrites of cortical neurons in the outer part of the molecular layer ( thalamic input leads to excitation of both pyramidal and nonpyramidal neurons in the cellular layer Larson-Prior et al, 1991).…”

“…Finally, pyramidal neurons in turtles also have local circuit excitatory connections, which appear to use both NMDA and non-NMDA-type glutamate receptors and nonglutamatergic receptors (Larson-Prior et al, 1991). In these various respects (the neuronal types present in cortex, their somatodendritic morphology, their electrophysiological characteristics, their connectivity with each other and with their thalamic input, and the neurotransmitter mechanisms involved), the fundamental features of the organization of turtle cortex are similar to those of mammalian cortex (Smith et al, 1980;Connors and Kriegstein, 1986;Kriegstein and Connors, 1986; Larson-Prior er al., 1991). Thus, the basic neuronal building blocks of the cortex and their functional properties are similar in turtles and mammals.…”

Evolutionary origin of Tbr2‐expressing precursor cells and the subventricular zone in the developing cortex

“…The three layers of turtle cortex include an outer molecular layer that contains some inhibitory interneurons, a pyramidal cell layer that consists primarily of excitatory pyramidal neurons, and a subcellular layer that is adjacent to the lateral ventricle and contains interneurons, some pyramidal cells, and GFAP-positive astroglial cells (Connors and Kriegstein, 1986;Blanton et al, 1987). The discrete cortical regions in turtle forebrain are readily distinguished in Nissl stained tissue, and include the medial cortex, dorsomedial cortex, dorsal cortex, lateral cortex, and the dorsal ventricular ridge (DVR) (Nieuwenhuys et al, 1998).…”