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Intracellular activity of morphologically identified neurons of the grass frog's optic tectum in response to moving configurational visual stimuli

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Summary

In the grass frogRana temporaria, various classes of tectal neurons were identified by means of intracellular recording and iontophoretic staining using potassium-citrate/Co3+-lysine-filled micropipettes, which have been defined previously by extracellular recording methods.

Class T5(1) neurons had receptive fields (RF) of 33°±5° diameter. In response to a moving 8°×8° square (S), a 2°×16° worm-like (W), or a 16°×2° antiworm-like (A) moving stripe, these cells showed excitatory postsynaptic potentials (EPSPs) and spikes which were interrupted occasionally by small inhibitory postsynaptic potentials (IPSPs). The excitatory responses (R) were strongest towards the square (RS) and less to the worm (RW). For the antiworm (RA) the responses were smallest or equal to the worm stimulus yielding the relationship RS>RW≧RA. Some of these cells were identified as pear-shaped or large ganglionic neurons, whose somata were located in the tectal cell layer 8. The somata of other large ganglionic neurons were found in layer 7 and the somata of other pear-shaped neurons at the top of layer 6, both displaying T5(1) properties.

Class T5(2) neurons (RF=34°±3°) responded with large EPSPs and spikes, often interrupted by small IPSPs, when their RF was traversed by the square stimulus. The excitatory activity was somewhat less to the worm stimulus, whereas no activity at all, or only IPSPs, were recorded in response to the antiworm-stimulus; thus yielding the relationship for the excitatory activity RS>RW>RA≈ 0. Such a cell was identified as pyramidal neuron; the soma was located at the top of layer 6, with the long axon travelling into layer 7 to the medulla oblongata.

Class T5(3) neurons (RF=29°±6°) showing EPSPs and spikes according to the relationship RS>RA>RW have been identified as large ganglionic neurons. Their somata were located in layer 8.

Class T5(4) neurons (RF=24±7°) responded only to the square stimulus with EPSPs and spikes, sometimes interrupted by IPSPs and yielding the relationship RS>RA≈RW≈0. The somata of these large ganglionic or pear-shaped neurons were located in layer 8.

Class T1(1) neurons (RF=30°–40°) were most responsive to stimuli moving at a relatively long distance in the binocular visual field, and have been identified as pear-shaped neurons. Their somata were located in layer 6.

Further neurons are described and morphologically identified which have not yet been classified by extracellular recording methods. For example,IPSP neurons (RF=20°–30°) responded (R′) with IPSPs only according to the relationship R′S>R′A≈ R′W. The somata of these pear-shaped neurons were located in layer 6.

The properties of tectal cells in response to electrical stimulation of the optic tract and to brisk changes of diffuse illumination suggest certain neuronal connectivity patterns. The results support the idea ofintegrative functional units (assemblies) of connected cells which are involved in various perceptual processes, such as configurational prey selection expressed by T5(2) prey-selective neurons.

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Abbreviations

A :

antiworm-like 16°×2° stripe stimulus with long axis perpendicular to the direction of movement

W :

wormlike 2°×16° stripe stimulus with long axis oriented parallel to the direction of movement

S :

square 8°×8° moving stimulus

ERF :

excitatory receptive field

IRF :

inhibitory receptive field

RF :

receptive field

EPSP :

excitatory postsynaptic potential

IPSP :

inhibitory postsynaptic potential

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Matsumoto, N., Schwippert, W.W. & Ewert, J.P. Intracellular activity of morphologically identified neurons of the grass frog's optic tectum in response to moving configurational visual stimuli. J. Comp. Physiol. 159, 721–739 (1986). https://doi.org/10.1007/BF00603726

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