Chattering and differential signal processing in identified motion-sensitive neurons of parallel visual pathways in the chick tectum

Abstract

At least three identified cell types in the stratum griseum centrale (SGC) of the chick optic tectum mediate separate pathways from the retina to different subdivisions of the thalamic nucleus rotundus. Two of these, SGC type I and type II, constitute the major direct inputs to rotundal subdivisions that process various aspects of visual information, e.g., motion and luminance changes. Here, we examined the responses of these cell types to somatic current injection and synaptic input. We used a brain slice preparation of the chick tectum and applied whole-cell patch recordings, restricted electrical stimulation of dendritic endings, and subsequent labeling with biocytin. Type I neurons responded with regular sequences of bursts ("chattering") to depolarizing current injection. Electrical stimulation of retinal afferents evoked a sharp-onset EPSP/burst response that was blocked with CNQX. The sharp-onset EPSP/burst response to synaptic stimulation persisted when the soma was hyperpolarized, thus suggesting the presence of dendritic spike generation. In contrast, the type II neurons responded to depolarizing current injection solely with an irregular sequence of individual spikes. Electrical stimulation of retinal afferents led to slow and long-lasting EPSPs that gave rise to one or several action potentials. In conclusion, the morphological distinct SGC type I and II neurons also have different response properties to retinal inputs. This difference is likely to have functional significance for the differential processing of visual information in the separate pathways from the retina to different subdivisions of the thalamic nucleus rotundus.

Fig. 1.

Schematic of the slice preparation.A, Overview of the transversal midbrain slice.Inset, The tectal area shown in B.B, Reconstruction of an SGC-I neuron superimposed on the tectal outline. Inset (right), The layers visible in a Nissl stain or with acridin-orange incubation in vitro. Note the positioning of the stimulation electrodes above and within the retinorecipient layer 5b (boxed area). C, Schematic of the spatial separation of the electrostimulation and the postsynaptic elements. Stimulated retinal afferents and the bottlebrush ending are outlined with thick lines; nonstimulated elements are outlined with thin lines. Cer, Cerebellum.

Fig. 2.

A, Digital image of soma, basal dendrites, and one bottlebrush ending (asterisk) of a biocytin-labeled SGC-I neuron viewed with differential interference contrast optics to show the tectal layering (layers 5b, 6, 8 indicated). B, C, Examples of bottlebrush endings of the same cell at higher magnification. Scale bars: A, 100 μm; B, C, 10 μm.

Fig. 3.

Reconstruction of an SGC-I neuron labeled with biocytin after whole-cell patch recording. The characteristics of this cell type include the large dendritic field, the position of the soma in the upper half of the SGC, and the arrangement of the bottlebrush dendritic endings in the retinorecipient layer 5b.

Fig. 4.

Somatic physiology of SGC-I neurons.A, Response to somatic current injection (0.4 nA). After a short burst at the onset containing two to four action potentials, the membrane potential remained constant. B, Response of the same neuron to stronger current injection (1.0 nA), showing the typical chattering behavior that contains bursts of action potentials (2–5) with regular interburst intervals. C, Chattering frequency plotted against injected current. Inset, Intraburst frequency plotted against injected current. Data shown are means ± SE. D, Depolarizing voltage sag evoked by a hyperpolarizing current pulse (−0.4 nA).

Fig. 5.

Response of SGC-I neurons to electrical stimulation of retinal afferents. A, Synaptic stimulation via electrical stimulation (1 msec; 400 μA) of retinal afferents with electrodes in layer 2–4 is shown. Inset, This response is completely abolished after incubation with 10 μm CNQX. B, Direct electrical stimulation (2 msec; 100 μA) of bottlebrush dendritic endings with electrodes in layer 5b is shown. Note the sharp onset of the cellular response evoked by either stimulation or the difference in latency.Inset, The same traces inB are shown with a higher time resolution.C, Comparable sharp-onset EPSP/burst responses to synaptic stimulation (1 msec; 100 μA) were elicited when the soma was hyperpolarized by current injection (−0.6 nA).

Fig. 6.

Reconstruction of an SGC-II neuron labeled with biocytin after whole-cell patch recording. This cell type is characterized by large dendritic fields, the position of the soma in the lower half of the SGC, and the position of bottlebrush dendritic endings below the retinorecipient layers.

Fig. 7.

Somatic physiology of SGC-II neurons.A, Response to somatic current injection (0.1 nA) consisting of single action potentials. B, Tonic response of the same neuron to stronger current injection (0.7 nA).C, Spike frequency of the tonic response plotted against injected current. Data shown are means ± SE. D, Depolarizing voltage sag evoked by a hyperpolarizing current pulse (−0.5 nA).

Fig. 8.

Response of SGC-II neurons to electrical stimulation of retinal afferents. A, Cells responded to synaptic stimulation (1 msec; 30 μA) with one to three action potentials riding on a broad EPSP. Inset, This response is completely abolished after incubation with 10 μm CNQX.B, In some cases, the response to synaptic stimulation (1 msec; 60 μA) lasted several hundred milliseconds.C, When the soma was hyperpolarized by current injection (−0.4 nA) during the delivery of the synaptic stimulus, cells typically responded to synaptic stimulation (1 msec; 60 μA) with an EPSP without spikes.