Nasotemporal overlap in visual field projected to lateral geniculate nucleus in the cat.
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Depth Perception↗
Biomedical subjects
S M Sherman
Publications and source records attributed to S M Sherman.
Memory consolidation of one-trial learning in chicks.
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Animals↗
Brain-stem modulation of the response properties of cells in the cat's perigeniculate nucleus.
Transmission through the lateral geniculate nucleus is facilitated following activation of the cholinergic input from the brain stem, which is thought to reflect activity patterns seen during arousal. One of the underlying mechanisms is the suppression of inhibitory circuits local to the lateral geniculate nucleus. However, evidence exists that some visually driven inhibitory inputs to geniculate nucleus. preserved or even enhanced under conditions of arousal, and during electrical activation of the parabrachial region of the brain stem. We have therefore reexamined the effect of brain-stem activation on the visual responses of one group of local inhibitory inputs to geniculate relay cells, those emanating from the adjacent perigeniculate nucleus. We recorded single perigeniculate cells in anesthetized, paralyzed cats. Axons innervating the lateral geniculate and perigeniculate nuclei from the parabrachial region of the brain stem were electrically activated, and the effect of this activation was assessed on both spontaneous and visually evoked responses. Visual stimulation consisted of sinusoidally modulated sine-wave gratings of varying spatial and temporal frequency. For the great majority of perigeniculate cells (32 of 40), brain-stem activation inhibited spontaneous activity, while one cell was excited, three showed a mixed effect and four were unaffected. Nevertheless, the responses of most cells (30 of 40) were facilitated when brain-stem activation was paired with certain spatio-temporal patterns of visual stimulation. Spatial tuning curves were constructed for 17 cells and temporal tuning curves for 14, before and during parabrachial activation. The responses of any one cell could be facilitated, unchanged, or suppressed, depending on the visual stimulus used. In some cases, this substantially modified the cell's spatial and temporal tuning properties. We conclude that activation of the brain stem disinhibits geniculate relay cells in the absence of visual stimulation, but it has the potential to enhance either the magnitude or specificity of visually driven inhibition arising from the perigeniculate nucleus.
Animals↗
The brain-stem parabrachial region controls mode of response to visual stimulation of neurons in the cat's lateral geniculate nucleus.
We recorded the responses of neurons from the cat's lateral geniculate nucleus to drifting sine-wave grating stimuli both before and during electrical stimulation of the parabrachial region of the midbrain. The parabrachial region provides a mostly cholinergic input to the lateral geniculate nucleus, and our goal was to study its effect on responses of geniculate cells to visual stimulation. Geniculate neurons respond to visual stimuli in one of two modes. At relatively hyperpolarized membrane potentials, low threshold (LT) Ca2+ spikes are activated, leading to high-frequency burst discharges (burst mode). At more depolarized levels, the low threshold Ca2+ spike is inactivated, permitting a more tonic response (relay or tonic mode). During our intracellular recordings of geniculate cells, we found that, at initially hyperpolarized membrane potentials, LT spiking in response to visual stimulation was pronounced, but that parabrachial activation abolished this LT spiking and associated burst discharges. Coupled with the elimination of LT spiking, parabrachial activation also led to a progressive increase in tonic responsiveness. Parabrachial activation thus effectively switched the responses to visual stimulation of geniculate neurons from the burst to relay mode. Accompanying this switch was a gradual depolarization of resting membrane potential by about 5-10 mV and a reduction in the hyperpolarization that normally occurs in response to the inhibitory phase of the visual stimulus. Presumably, the membrane depolarization was sufficient to inactivate the LT spikes. We were able to extend and confirm our intracellular observations on the effects of parabrachial activation to a sample of cells recorded extracellularly. This was made possible by adopting empirically determined criteria to distinguish LT bursts from tonic responses solely on the basis of the temporal pattern of action potentials. During parabrachial activation, every cell responded only in the relay mode, an effect that corresponds to our intracellular observations. We quantified the effects of parabrachial activation on various response measures. The fundamental Fourier response amplitude (F1) was calculated separately for the total response, the tonic response component, and the LT burst component. Parabrachial activation resulted in an increased F1 amplitude for the total response. This increase was due to an increase in the tonic response component. For a subset of cells showing epochs of LT bursting, parabrachial activation concurrently reduced LT bursting and increased the amplitude of the tonic response. Parabrachial activation, by eliminating LT bursting, also caused cells to respond with more linearity.(ABSTRACT TRUNCATED AT 400 WORDS)
Animals↗
Dual response modes in lateral geniculate neurons: mechanisms and functions.
Relay cells of the lateral geniculate nucleus, like those of other thalamic nuclei, manifest two distinct response modes, and these represent two very different forms of relay of information to cortex. When relatively hyperpolarized, these relay cells respond with a low threshold Ca2+ spike that triggers a brief burst of conventional action potentials. These cells switch to tonic mode when depolarized, since the low threshold Ca2+ spike, being voltage dependent, is inactivated at depolarized levels. In this mode they relay information with much more fidelity. This switch can occur under the influence of afferents from the visual cortex or parabrachial region of the brain stem. It has been previously suggested that the tonic mode is characteristic of the waking state while the burst mode signals an interruption of the geniculate relay during sleep. This review surveys the key properties of these two response modes and discusses the implications of new evidence that the burst mode may also occur in the waking animal.
Action Potentials↗
Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode.
Relay cells of the lateral geniculate nucleus respond to visual stimuli in one of two modes: burst and tonic. The burst mode depends on the activation of a voltage-dependent, Ca2+ conductance underlying the low threshold spike. This conductance is inactivated at depolarized membrane potentials, but when activated from hyperpolarized levels, it leads to a large, triangular, nearly all-or-none depolarization. Typically, riding its crest is a high-frequency barrage of action potentials. Low threshold spikes thus provide a nonlinear amplification allowing hyperpolarized relay neurons to respond to depolarizing inputs, including retinal EPSPs. In contrast, the tonic mode is characterized by a steady stream of unitary action potentials that more linearly reflects the visual stimulus. In this study, we tested possible differences in detection between response modes of 103 geniculate neurons by constructing receiver operating characteristic (ROC) curves for responses to visual stimuli (drifting sine-wave gratings and flashing spots). Detectability was determined from the ROC curves by computing the area under each curve, known as the ROC area. Most cells switched between modes during recording, evidently due to small shifts in membrane potential that affected the activation state of the low threshold spike. We found that the more often a cell responded in burst mode, the larger its ROC area. This was true for responses to optimal and nonoptimal visual stimuli, the latter including nonoptimal spatial frequencies and low stimulus contrasts. The larger ROC areas associated with burst mode were due to a reduced spontaneous activity and roughly equivalent level of visually evoked response when compared to tonic mode. We performed a within-cell analysis on a subset of 22 cells that switched modes during recording. Every cell, whether tested with a low contrast or high contrast visual stimulus exhibited a larger ROC area during its burst response mode than during its tonic mode. We conclude that burst responses better support signal detection than do tonic responses. Thus, burst responses, while less linear and perhaps less useful in providing a detailed analysis of visual stimuli, improve target detection. The tonic mode, with its more linear response, seems better suited for signal analysis rather than signal detection.
Animals↗
Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys.
Thalamic relay cells fire in two distinct modes, burst or tonic, and the operative mode is dictated by the inactivation state of low-threshold, voltage-gated, transient (or T-type) Ca2+ channels. Tonic firing is seen when the T channels are inactivated via membrane depolarization, and burst firing is seen when the T channels are activated from a hyperpolarized state. These response modes have very different effects on the relay of information to the cortex. It had been thought that only tonic firing is seen in the awake, alert animal, but recent evidence from several species suggests that bursting may also occur. We have begun to explore this issue in macaque monkeys by recording from thalamic relay cells of unanesthetized, behaving animals. In the lateral geniculate nucleus, the thalamic relay for retinal information, we found that tonic mode dominated responses both during alert behavior as well as during sleep. We nonetheless found burst firing present during the vigilant, waking state. There was, however, considerably more burst mode firing during sleep than wakefulness. Surprisingly, we did not find the bursting during sleep to be rhythmic. We also recorded from relay cells of the somatosensory thalamus. Interestingly, not only did these somatosensory neurons exhibit much more burst mode activity than did geniculate cells, but bursting during sleep was highly rhythmic. It thus appears that the level and nature of relay cell bursting may not be constant across all thalamic nuclei.
Action Potentials↗
The effects of saccadic eye movements on the activity of geniculate relay neurons in the monkey.
Saccadic suppression is the reduced visibility that occurs during saccadic eye movements. Recent psychophysical studies have suggested that this is due to a reduction in responsiveness of magnocellular (M), but not parvocellular (P), cells of the lateral geniculate nucleus. To address this and other phenomena of responsiveness during saccades, we recorded from geniculate neurons in the behaving monkey before, during, and after saccades. Specifically, we measured neuronal responses to a flashing, whole-field illumination. Contrary to the prediction, most M neurons showed pronounced enhancement of visual activity during saccades, whereas such responsiveness of parvocellular (P) neurons was not significantly affected by saccades. We also analyzed the extent to which saccades affected burst firing, which results from activation of a voltage-dependent Ca2+ conductance. We found that both M and P cells displayed a significant suppression of burst firing during saccades. These results do not support the idea that saccadic suppression has an obvious substrate in reduced responsiveness of geniculate cells, but this suppression may be related to an increased visual threshold for detection associated with reduced burst firing.
Action Potentials↗
Response latencies of cells in the cat's lateral geniculate nucleus are less variable during burst than tonic firing.
We measured the variability in latency of the first spike seen in cells of the cat's lateral geniculate nucleus following the onset of a visual stimulus. We found that, in each of the 11 cells tested, this variability was significantly lower during burst than during tonic firing. We suggest that this difference confers an advantage in signal detection during burst compared to tonic firing. This complements other reported advantages of burst firing for signal detection seen in signal-to-noise ratios and in the ability to efficiently drive postsynaptic cells.
Action Potentials↗
Development of X- and Y-cell retinogeniculate terminations in kittens.
The cat retinogeniculocortical pathways are organized chiefly into two parallel independent neuronal streams, one involving X-cells of the retina and lateral geniculate nucleus, and the other, Y-cells. Development of the Y-cell pathway is more seriously affected by visual deprivation than is the X-cell pathway and we reasoned that some insight into the underlying mechanisms of these effects could be gained from studies of normal development. We therefore injected horseradish peroxidase into physiologically identified X- and Y-cell retinogeniculate axons to examine the postnatal development of their terminations in kittens. As we report here, at 3-4 weeks of age, most optic tract axons can be identified physiologically as members of the X- or Y-cell class. X-cell terminal fields in lamina A or A1 are wider at 3-4 weeks than they are in adults, while Y-cell terminal fields are narrower than in adults. During the second and third postnatal months, X-cell terminal arbors progressively contract while Y-cell arbors expand so that, by 12 weeks of age, the adult pattern is seen. These data, and the results of our earlier study of the effects of monocular lid suture on these terminal arbors, suggest that enlargement of Y-cell terminations in geniculate lamina A or A1 during development may be accompanied by competitive pruning of X-cell terminations within these same laminae.
Animals↗
Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat.
Although receptive fields of relay cells in the lateral geniculate nucleus of the cat nearly match those of their retinal afferents, only 10-20% of the synapses on these cells derive from the retina and are excitatory. Many more (30-40%) are inhibitory and largely control the gating of retinogeniculate transmission. These inhibitory synapses derive chiefly from two cell types: intrinsic local circuit neurones and cells in the adjacent perigeniculate nucleus. It has been difficult to study the functional organization of these inhibitory pathways; most efforts have relied on indirect approaches. Here we describe the use of direct techniques to study a local circuit neurone by iontophoresing horseradish peroxidase (HRP) into it, which completely labels the soma and processes of cells for subsequent light- and electron microscopic analysis. Although the response properties of the labelled cell are virtually indistinguishable from those of many relay cells, its morphology is typical of 'class 3' neurones (see Fig. 1 legend), which are widely believed to be interneurones (but see ref. 12). Here, we refer to the cell as a 'local circuit neurone', which allows for the possibility of a projection axon, rather than as an 'interneurone', a term that commonly excludes a projection axon. We find that the labelled cell has a myelinated axon, but that the axon loses its myelin within 50 microns of the soma and has not yet been traced further. The dendrites of the labelled cell possess presynaptic terminals that act as intrinsic sources of inhibition on geniculate relay cells. We also characterize other morphological aspects of this inhibitory circuitry.
Animals↗