Cellular physiology of the turtle visual cortex: synaptic properties and intrinsic circuitry

Abstract

We have examined the synaptic physiology of the isolated dorsal cortex of the turtle, Pseudemys scripta elegans. Electrical stimulation of afferent pathways elicited distinct, stereotyped responses in pyramidal and stellate neurons. Single shocks evoked a long-lasting barrage of excitatory postsynaptic potentials (EPSPs) in stellate cells, and led to a burst of several action potentials. Under the same circumstances, pyramidal cells displayed a small amount of short-latency excitation, but this was accompanied by a profound and prolonged set of inhibitory post-synaptic potentials (IPSPs). Synaptic excitation of the distal dendrites of pyramidal cells could evoke dendritic action potentials that were visible at the soma as small all-or-none spikes rising from the hyperpolarized level of the IPSP. There appeared to be two mechanistically different types of IPSPs in pyramidal cells. The first occurred at short latency, could produce a very large conductance increase, reversed polarity at -71 mV, and was chloride-dependent. The second was generally smaller and more protracted, had a relatively negative reversal potential of -85 to -95 mV, and was insensitive to chloride injection. Focal application of small doses of the putative inhibitory neurotransmitter gamma-aminobutyric acid (GABA) onto the somata of pyramidal cells caused a conductance increase and hyperpolarization. This response had features in common with the short-latency IPSP, including an identical reversal potential. Application of large doses of GABA to the somata of pyramidal cells or smaller doses to their dendrites elicited multiphasic or purely depolarizing responses that were at least partly due to time- or space-dependent shifts of the equilibrium potential of the response. Bicuculline methiodide, a potent GABA antagonist, depressed both the responses to GABA and the short-latency IPSP, but not the long-latency IPSP; synchronized epileptiform burst discharges also resulted. These findings, together with responses to locally applied electric shocks and the excitatory amino acid glutamate, suggested that inhibition of pyramidal cells was generated intrinsically by stellate cells, and that the cortical circuit provides pathways for both feedforward and feedback GABAergic inhibition. The data also suggest that pyramidal cells are mutually excitatory. These features are similar to the basic intrinsic circuitry in the telencephalic cortices of mammals.

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

“…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.…”

“…The available studies thus far indicate that turtle dorsal cortex shares many similarities with mammalian isocortex, but seems to correspond most closely to layers 5-6 of mammalian cortex. Thus, anatomical and physiological studies of turtles cortex could shed light on the neurotransmitter and synaptic mechanisms underlying intemeuronal communication in cortex, at least those having to do with fundamental processing occurring in infragranular cortex Kriegstein and Connors, 1986;Larson-Prior et al, 1991). One particularly exciting area of synaptic physiology in which study of turtle cortex could be useful is &hernia.…”

“…Elucidating the basis of the unique resistance of turtle cortex to ischemia may provide clues for combating ischemic neuronal death in humans (Young et al, 1990). Finally, turtle nervous system in general is a favorable model for neurophysiological study because it readily lends itself to use as an extremely durable in vitro preparation Kriegstein and Connors, 1986;Larson-Prior et al, 1991).…”

Differential effect of zinc on the vertebrate GABAA‐receptor complex

“…The position of the GABA pipette was adjusted until a 3-15s GABA application (1I303nA) evoked consistent, brief depolarizations at the resting membrane potential (typically -80 mV for olfactory neurones). Higher ejection currents for more prolonged periods were avoided to minimize any shifts in the GABA equilibrium potential or overt GABA receptor desensitization (Kriegstein & Connors, 1986). Data were recorded on a Brush-Gould 2400 chart recorder.…”

Visual stimuli induce waves of electrical activity in turtle cortex

“…The flow of visual information through the retinogeniculocortical pathway in turtles projects to a rostral area of its dorsal cortex (1,2), whose cellular and synaptic physiology share basic features with mammalian neocortex (3,4). Anatomical studies indicate that the geniculocortical afferents traverse the lateral part of this area of dorsal cortex with few collaterals, and their ending defines the border between a lateral, solely visual area (D2) and a medial area (D1) that receives input from multiple sensory modalities (2,5) (Fig.…”