Evidence for excitatory connections from the deprived eye to the visual cortex in monocularly deprived kittens.
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Biomedical subjects
Publications and source records attributed to T Tsumoto.
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1. In the cat visual cortex (VC), electrophoretic glutamate application at a depth corresponding to layer VI may have excitatory or inhibitory effects on relay cells of the lateral geniculate nucleus (LGN). Corticofugal excitation was seen, if the receptive field centers (RFCs) of the VC neurons recorded at the application site were within 2.3 degrees of the RFCs of the LGN neurons under test. Inhibitory effects were seen if the RFCs of both cells were further apart up to 3.1 degrees. Glutamate application at more superficial cortical sites had no effect on LGN-neuron activity. 2. Cross-correlation analysis between spontaneous activities of simultaneously recorded VC and LGN neurons revealed excitatory cortico-geniculate connections in 18 pairs with RFCs separated by less than 1.7 degrees. In 15 pairs the peak latency of the excitation was 2--5 msec (3.4 msec in the average), 3 pairs showed long cortico-geniculate latencies (13--18 msec). The existence of a fast and slow cortico-geniculate system is suggested. 3. Inhibitory cortico-geniculate interaction was demonstrated with cross-correlation analysis in 8 pairs of which 4 had RFCs separated by more than 1.7 degrees. The onset latency of the inhibition was 2--7 msec except for 2 pairs with about 20 msec latency. 4. Most of the LGN neurons which were affected by cortical glutamate application or which showed an excitatory or inhibitory connection with a VC neurons were sustained cells, while the majority of VC neurons which were recorded in the effective glutamate application sites or which showed a significant interaction with LGN neurons in the cross-correlogram were binocularly driven and complex, with mostly large RFCs (mean diameter 3.5 degrees). They responded briskly to moving small spots as well as to moving slits. 5. It is concluded that the corticofugal excitatory effect is transmitted through monosynaptic links from VC neurons located in layer VI (complex cell) to LGN relay neurons (mostly sustained-cell) and this system is organized in a precise topographical manner. 6. In an Appendix neuron pairs which showed a positive correlation in the geniculo-cortical direction were described. The findings may support the view that complex as well as simple cells are drive monosynaptically from geniculo-cortical afferents of the sustained or transient type.
Effects of electrical stimulation of the frontal eye field (FEF) upon activites of the lateral geniculate body (LG) were studied in encephale isole cats. In some experiments the effects were examined by recording field responses of the dorsal nucleus of LG (LGd) and the visual cortex (VC) to electrical stimulation of the optic chiasm (OX). Conditioning repetitive stimulation of FEF exerted no significant effects on the r1 wave of LGd responses but had a facilitatory effect on the r2 wave. FEF-induced facilitation of VC responses was prominent in the late postsynaptic components. These effects had latencies of 50-100 msec and durations of 200-500 msec. Transection of the midbrain showed that most of the FEF-effect was not mediated via the brainstem reticular formation. Extracellular unitary recordings were made from 125 neurons, of which 91 were LGd neurons, 23 neurons of the caudal part of the thalamic reticular nucleus (TRc) and 11 neurons of the ventral nucleus of LG (LGv). In 30 to 87 LGd relay neurons FEF stimuli increased response probabilities to OX stimuli and their spontaneous discharges. These FEF-facilitated LGd neurons were distinguished from the non-affected ones in that the former had longer OX-latencies than the latter. The FEF-facilitated neurons probably correspond to "X" neurons of LGd. In 17 TRc neurons the effects were inhibitory. Their time courses were similar to those of the facilitation in the LGd relay neurons. Seven LGv neurons recieved facilitaroy effects from FEF. Among them 5 neurons showed short-latency (6.7-17 msec) responses to FEF single shocks. The FEF sites inducing conjugate lateral eye movements exerted stronger facilitatory effects than those inducing upward or centering eye movements did. It is suggested that the effects may subserve to cancel the inhibitory convergence onto X-cells just after saccadic eye movements so as to improve visual information transmission through LGd during the eye fixation.
In the thalamic ventrobasal complex (VB) of the cat, effects of electrical stimulation of the pyramidal tract (PT) upon activities of 112 relay cells and 18 internuncial cells were examined. Single PT shocks to the cerebral peduncle elicited short-latency discharges in 31 relay cells (mean latency, 1.4 +/- 0.5 msec). When weak PT stimuli were employed as conditioning shocks, facilitatory effects upon responses to medial lemniscal (ML) stimulation were observed. It was revealed that VB relay cells were excited monosynaptically via collaterals of the fast PT fibers. Among 31 PT-excited cells 22 were fired by movements of joints (joint-movement units) and they made up 88% of all the joint-movement units. A majority of the relay cells responding to stimulation of hairs (hair units) did not receive excitatory effects from PT, except some special ones which represented long hairs at the distal or proximal end of the forearm-forepaw. In 44 relay cells repetitive PT shocks suppressed both evoked responses to ML stimulation and spontaneous discharges for 70--100 msec. Of these, 34 were hair units. The PT-induced inhibition in the hair units increased as their receptive fields shifted from the trunk towards the digits. Some intracellular recordings showed that the PT-induced inhibition was due to IPSPs generated disynaptically. Among 18 interneurons presumed to be inhibitory 10 responded with short latencies to PT stimulation. These were mostly the interneurons which presumably subserve the recurrent collateral inhibition in VB.
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Acidic amino acids, such as glutamate and aspartate, are thought to be excitatory transmitters in the cerebral neocortex and hippocampus. Receptors for these amino acids can be classified into at least three types on the basis of their agonists. Quisqualate-preferring receptors and kainate-preferring receptors are implicated in the mediation of synaptic transmission in many regions including the hippocampus and visual cortex, whereas N-methyl-D-aspartate (NMDA)-preferring receptors are thought to be involved in modulating synaptic efficacy, for example in longterm potentiation, a form of synaptic plasticity in the hippocampus. In the visual cortex of the cat and monkey, it is well established that synaptic plasticity, estimated by susceptibility of binocular responsiveness of cortical neurons to monocular visual deprivation, disappears after the 'critical' period of postnatal development. Here we report that during the critical period in young kittens, a selective NMDA-receptor antagonist blocks visual responses of cortical neurons much more effectively than it does in the adult cat. This suggests that NMDA receptors may be involved in establishing synaptic plasticity in the kitten visual cortex.
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