Cat Lateral Geniculate Nucleus Research Articles

Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus.

The role of the lateral geniculate nucleus (LGN) of the thalamus in visual encoding remains an open question. Here, we characterize the function of tonic and burst spikes in cat LGN X-cells in signaling features of natural stimuli. A significant increase in bursting was observed during natural stimulation (relative to white noise stimulation) and was linked to the strong correlation structure of the natural scene movies. Burst responses were triggered by specific stimulus events consisting of a prolonged inhibitory stimulus, followed by an excitatory stimulus, such as the movement of an object into the receptive field. LGN responses to natural scene movies were predicted using an integrate-and-fire (IF) framework and compared with experimentally observed responses. The standard IF model successfully predicted LGN responses to natural scene movies during tonic firing, indicating a linear relationship between stimulus and response. However, the IF model typically underpredicted the LGN response during periods of bursting, indicating a nonlinear amplification of the stimulus in the actual response. The addition of a burst mechanism to the IF model was necessary to accurately predict the entire LGN response. These results suggest that LGN bursts are an important part of the neural code, providing a nonlinear amplification of stimulus features that are typical of the natural environment.

How much feedback from visual cortex to lateral geniculate nucleus in cat: A perspective

Corticothalamic feedback is believed to play an important role in selectively regulating the flow of sensory information from thalamus to cortex. But despite its importance, the size and nature of corticothalamic pathway connectivity is not fully understood. In light of recent empirical data, the aim of this paper was to quantify the contribution of area 17 axon connectivity to the synaptic organization of A-laminae in dorsal lateral geniculate nucleus (dLGN) in cat, the best studied corticothalamic pathway. Numerical constraints indicate that most corticogeniculate synapses are not formed with inhibitory interneurons. However, the main finding is that there was an order of magnitude difference between estimates of the mean number of cortical synapses per A-laminae neuron based on individual corticogeniculate axon data (12,000-16,000 cortical synapses per cell) than that previously derived from partial reconstructions of the synaptic input to two physiologically identified relay cells (1200-1500 cortical synapses per cell). In an attempt to reconcile these different estimates, parameter variation and comparative analyses suggest that previous work may have overestimated the density of corticogeniculate efferent neurons and underestimated the total number of synapses per geniculate neuron. But as this analysis did not include area 18 corticogeniculate axons innervating A-laminae, the discrepancy between different estimates may be greater and require further explanation. Thus, the analysis presented here suggests geniculate neurons receive on average a greater number of cortical synapses per cell but from far fewer corticogeniculate axons than previously thought.

Three bands of oscillatory activity in the lateral geniculate nucleus of the cat visual system*1

Neuronal responses in the cat lateral geniculate nucleus were analyzed with respect to oscillatory components in 5930 peri-stimulus time histograms recorded in 69 neurons. Oscillatory components were observed in three frequency ranges clearly separated from each other, i.e. in a lower range between 25 and 33 Hz (mean 27.8 Hz), in a middle range between 45 and 60 Hz (mean 52.5 Hz), and in a higher range between 75 and 100 Hz (mean 84.4 Hz); temporal variance within the neuronal populations showing oscillatory characteristics increased with higher frequencies. Although the frequency ranges of the oscillatory responses were clearly separated from each other, a functional dependence between these three populations of geniculate neurons appears to be possible; the numerical relationship of approximately 1:2:3 points to the possibility of a temporal coupling between distinct neuronal populations at an early stage of visual processing.

Three bands of oscillatory activity in the lateral geniculate nucleus of the cat visual system

Neuronal responses in the cat lateral geniculate nucleus were analyzed with respect to oscillatory components in 5930 peri-stimulus time histograms recorded in 69 neurons. Oscillatory components were observed in three frequency ranges clearly separated from each other, i.e. in a lower range between 25 and 33 Hz (mean 27.8 Hz), in a middle range between 45 and 60 Hz (mean 52.5 Hz), and in a higher range between 75 and 100 Hz (mean 84.4 Hz); temporal variance within the neuronal populations showing oscillatory characteristics increased with higher frequencies. Although the frequency ranges of the oscillatory responses were clearly separated from each other, a functional dependence between these three populations of geniculate neurons appears to be possible; the numerical relationship of approximately 1:2:3 points to the possibility of a temporal coupling between distinct neuronal populations at an early stage of visual processing.

Discovering spike patterns in neuronal responses.

When a cortical neuron is repeatedly injected with the same fluctuating current stimulus (frozen noise) the timing of the spikes is highly precise from trial to trial and the spike pattern appears to be unique. We show here that the same repeated stimulus can produce more than one reliable temporal pattern of spikes. A new method is introduced to find these patterns in raw multitrial data and is tested on surrogate data sets. Using it, multiple coexisting spike patterns were discovered in pyramidal cells recorded from rat prefrontal cortex in vitro, in data obtained in vivo from the middle temporal area of the monkey (Buracas et al., 1998) and from the cat lateral geniculate nucleus (Reinagel and Reid, 2002). The spike patterns lasted from a few tens of milliseconds in vitro to several seconds in vivo. We conclude that the prestimulus history of a neuron may influence the precise timing of the spikes in response to a stimulus over a wide range of time scales.

Effects of short-term IOP elevation on receptive field properties of cat LGN cells

To investigate the effects of short-term intraocular pressure (IOP) elevation on the receptive field properties of lateral geniculate nucleus (LGN) cells, responses of the LGN cells to annulus, disc and drifting gratings with high or low spatial frequencies have been recorded extracellularly in the cat with the retinal perfusion pressure kept stable (30 mmHg). Our results indicated that the responses of the X and Y type LGN cells were significantly weakened during IOP elevation. And the responses varied with the different mechanisms of receptive fields. Specifically, while using annulus and disc as stimuli, the responses of Y cells were more tolerant than X cells to IOP elevation. The surround area of the receptive field was more sensitive to IOP elevation than the center. The mean responses during IOP elevation decreased more than the peak responses did. IOP elevation has more influence on the responses of X cells than on the response of Y cells to the drifting gratings with high spatial frequency. These results may reflect different degrees of ischemia on corresponding retinal structures caused by IOP elevation.

Linear mechanistic models for the dorsal lateral geniculate nucleus of cat probed using drifting-grating stimuli.

Experiments with sinusoidal visual stimuli in the early visual pathway have traditionally been interpreted in terms of descriptive filter models. We present an alternative mechanistic approach for interpretation of this type of data recorded from X cells in the dorsal lateral geniculate nucleus (dLGN) of cat. A general, linear, rate-based mathematical expression for the geniculate transfer ratio, i.e. the ratio between the first-harmonic components of the output of a geniculate relay cell and its retinal input, is derived. In linear theory this ratio is independent of the signal processing occurring at the retinal level. Further, the ratio is straightforwardly accessible in experiments due to the presence of S-potentials, representing the retinal input, in extracellular recordings from dLGN. The expression accounts for feedforward inputs from retina and intrageniculate interneurons as well as feedback inputs from cortex and the thalamic reticular nucleus and can be used to experimentally test different mechanistic models for the geniculate circuitry. Two examples of this are considered: a purely feedforward model incorporating relay cell inputs from retinal ganglion cells and interneurons, and a model including cortical feedback inhibition of relay cells via intrageniculate interneurons.

Brainstem modulation of visual response properties of single cells in the dorsal lateral geniculate nucleus of cat.

The dorsal lateral geniculate nucleus (dLGN) transmits visual signals from the retina to the cortex. In the dLGN the antagonism between the centre and the surround of the receptive fields is increased through intrageniculate inhibitory mechanisms. Furthermore, the transmission of signals through the dLGN is modulated in a state-dependent manner by input from various brainstem nuclei including an area in the parabrachial region (PBR) containing cholinergic cells involved in the regulation of arousal and sleep. Here, we studied the effects of increased PBR input on the spatial receptive field properties of cells in the dLGN. We made simultaneous single-unit recordings of the input to the cells from the retina (S-potentials) and the output of the cells to the cortex (action potentials) to determine spatial receptive field modifications generated in the dLGN. State-dependent modulation of the spatial receptive field properties was studied by electrical stimulation of the PBR. The results showed that PBR stimulation had only a minor effect on the modifications of the spatial receptive field properties generated in the dLGN. The PBR-evoked effects could be described mainly as increased response gain. This suggested that the spatial modifications of the receptive field occurred at an earlier stage of processing in the dLGN than the PBR-controlled gain regulation, such that the PBR input modulates the gain of the spatially modified signals. We propose that the spatial receptive field modifications occur at the input to relay cells through the synaptic triades between retinal afferents, inhibitory interneurone dendrites, and relay cell dendrites and that the gain regulation is related to postsynaptic cholinergic effects on the relay cells.

Completing the corticofugal loop: a visual role for the corticogeniculate type 1 metabotropic glutamate receptor.

The way in which the brain deals with sensory information relies not only on feedforward processing of signals from the periphery but also on feedback inputs. This is the case of the massive projection back from layer 6 in the visual cortex to the thalamus, for which, despite being the greatest single source of synaptic contacts, the functional role still remains unclear. In the cat lateral geniculate nucleus, part of this cortical feedback is mediated by type 1 metabotropic glutamate receptors (mGluR1s), which are exclusively located on distal segments of the relay-cell dendrites. Here we show that in adult cats the cortex uses a synaptic drive mediated by these receptors (mGluR1) specifically to enhance the excitatory center of the thalamic receptive field. Moreover the effect is maximum in response to those stimuli that effectively drive cortical cells, and importantly, it does not affect the spatiotemporal structure of the thalamic receptive field. Therefore, cortex, by closing this corticofugal "loop," is able to increase the gain of its thalamic input within a focal spatial window, selecting key features of the incoming signal.

Completing the Corticofugal Loop: A Visual Role for the Corticogeniculate Type 1 Metabotropic Glutamate Receptor

The way in which the brain deals with sensory information relies not only on feedforward processing of signals from the periphery but also on feedback inputs. This is the case of the massive projection back from layer 6 in the visual cortex to the thalamus, for which, despite being the greatest single source of synaptic contacts, the functional role still remains unclear. In the cat lateral geniculate nucleus, part of this cortical feedback is mediated by type 1 metabotropic glutamate receptors (mGluR1s), which are exclusively located on distal segments of the relay-cell dendrites. Here we show that in adult cats the cortex uses a synaptic drive mediated by these receptors (mGluR1) specifically to enhance the excitatory center of the thalamic receptive field. Moreover the effect is maximum in response to those stimuli that effectively drive cortical cells, and importantly, it does not affect the spatiotemporal structure of the thalamic receptive field. Therefore, cortex, by closing this corticofugal “loop,” is able to increase the gain of its thalamic input within a focal spatial window, selecting key features of the incoming signal.

D1 and D2 receptor-mediated dopaminergic modulation of visual responses in cat dorsal lateral geniculate nucleus.

The modulatory effects of dopamine (DA) on the visual responses of relay cells of the dorsal aspect of cat lateral geniculate nucleus (dLGN) were tested using local micro-iontophoretic application of DA and application of the receptor-specific agonists SKF38393 (SKF, D1/D5) and quinpirole (QUIN, D2/D3/D4) in the anaesthetized alcuronium-treated cat. The effects of DA and QUIN were clearly dose-dependent: small amounts caused a weak and transient facilitation of visual activity (10-30% increase) preferentially in Y-type relay cells, which changed to a moderate reduction of visual responses when the dose was increased (50%, maximal 70%). The effect of SKF was mainly suppressive and increased with the amount of drug applied (up to 90% reduction). The selective antagonists SCH23390 (SCH, D1) and sulpiride (SULP, D2) reduced the effects of co-applied DA agonists. We found little evidence for a specific dopaminergic modulation of the surround inhibition (stimulus-driven lateral inhibition) although DA slightly facilitated the transmission of weak signals (small stimuli). Nevertheless, some dopaminergic effects seem to be mediated via inhibitory interneurons regulating the strength of sustained or recurrent inhibition. Application of DA agonists during blockade of GABA(A) receptors indicates a direct suppression of relay cells via D1 receptors, an excitation of relay cells via D2 receptors and--with increasing amounts of D2 agonist--probably also an excitation of inhibitory interneurons, which results in an indirect inhibition of dLGN relay cells (predominantly of the X-type). The results are discussed in relation to the impairment of visual functions in Parkinson's disease.

Linear mechanistic models for the dorsal lateral geniculate nucleus of cat probed using drifting-grating stimuli

Experiments with sinusoidal visual stimuli in the early visual pathway have traditionally been interpreted in terms of descriptive filter models. We present an alternative mechanistic approach for interpretation of this type of data recorded from X cells in the dorsal lateral geniculate nucleus (dLGN) of cat. A general, linear, rate-based mathematical expression for the geniculate transfer ratio, i.e. the ratio between the first-harmonic components of the output of a geniculate relay cell and its retinal input, is derived. In linear theory this ratio is independent of the signal processing occurring at the retinal level. Further, the ratio is straightforwardly accessible in experiments due to the presence of S-potentials, representing the retinal input, in extracellular recordings from dLGN. The expression accounts for feedforward inputs from retina and intrageniculate interneurons as well as feedback inputs from cortex and the thalamic reticular nucleus and can be used to experimentally test different mechanistic models for the geniculate circuitry. Two examples of this are considered: a purely feedforward model incorporating relay cell inputs from retinal ganglion cells and interneurons, and a model including cortical feedback inhibition of relay cells via intrageniculate interneurons.

Variability and information in a neural code of the cat lateral geniculate nucleus.

A central theme in neural coding concerns the role of response variability and noise in determining the information transmission of neurons. This issue was investigated in single cells of the lateral geniculate nucleus of barbiturate-anesthetized cats by quantifying the degree of precision in and the information transmission properties of individual spike train responses to full field, binary (bright or dark), flashing stimuli. We found that neuronal responses could be highly reproducible in their spike timing (approximately 1-2 ms standard deviation) and spike count (approximately 0.3 ratio of variance/mean, compared with 1.0 expected for a Poisson process). This degree of precision only became apparent when an adequate length of the stimulus sequence was specified to determine the neural response, emphasizing that the variables relevant to a cell's response must be controlled to observe the cell's intrinsic response precision. Responses could carry as much as 3.5 bits/spike of information about the stimulus, a rate that was within a factor of two of the limit the spike train could transmit. Moreover, there appeared to be little sign of redundancy in coding: on average, longer response sequences carried at least as much information about the stimulus as would be obtained by adding together the information carried by shorter response sequences considered independently. There also was no direct evidence found for synergy between response sequences. These results could largely, but not entirely, be explained by a simple model of the response in which one filters the stimulus by the cell's impulse response kernel, thresholds the result at a fairly high level, and incorporates a postspike refractory period.

Temporal properties of pattern adaptation of relay cells in the lateral geniculate nucleus of cats

The temporal properties of pattern adaptation of relay cells induced by repeated sinusoidal drifting grating were investigated in the dorsal lateral geniculate nucleus (dLGN) of cats. The results showed that the response amplitude declined and the response latency prolonged when relay cells were pattern-adapted in dLGN, like the similar findings in visual cortex. However, in contrast to the result in cortex, the response phase of relay cells advanced. This implies that an inhibition with relatively long latency may participate in the pattern adaptation of dLGN cells and the adaptation in dLGN may be via a mechanism different from that of visual cortex.

Changes of contrast gain in cat dorsal lateral geniculate nucleus by dopamine receptor agonists

The modulatory effects of dopamine (DA) on the contrast gain of retino-geniculate transmission were tested with local micro-iontophoretical application of DA and the DA receptor agonists SKF38393 (SKF, D1/D5) and quinpirole (QUIN, D2/D3/D4) while recording visually induced spike activity of relay cells of the dorsal aspect of cat lateral geniculate nucleus (dLGN) in the anesthetised and paralyzed preparation. DA and QUIN could either facilitate or inhibit visual activity in a dose-dependent fashion: small amounts caused a facilitation while larger quantities resulted in a more (DA) or less (QUIN) strong inhibition. The effect of SKF was almost always suppressive and increased with the amount of drug applied. The absolute change in activity was depending on stimulus contrast and the strength of the elicited response: facilitation and inhibition of activity was proportional to stimulus contrast and response strength and thus resulted in a changed contrast gain. The results indicate that the visual deficits found in Parkinson's disease patients my be not solely related to retinal dysfunctions.

Activation of γ-aminobutyric acid B receptors by baclofen improves visual temporal property of relay cells in the cat lateral geniculate nucleus

The role of γ-aminobutyric acid B (GABA B) receptors in spatial and temporal properties of the neurons was investigated in the cat dorsal lateral geniculate nucleus (dLGN) using flashing spot and drifting grating stimuli. Iontophoresis of baclofen, the selective GABA B receptor agonist significantly decreased the spontaneous and visual evoked responses (decreased to 38±7%), in which only the sustained component was suppressed sharply. Baclofen affected neither the center-surround antagonism of receptive fields nor the optimal spatial frequency of stimulating gratings. However, baclofen shortened cells’ response duration and elevated their temporal frequencies that evoked the maximum and the half maximum response. In contrast, 2-OH-sacrofen, a GABA B antagonist showed no significant effect on dLGN cells’ spatio-temporal properties. In conclusion, the activation of GABA B receptors may improve the temporal response properties of dLGN cells’ via the sustained pathway, rather than change the spatial properties.

Dynamics of Low-Threshold Spike Activation in Relay Neurons of the Cat Lateral Geniculate Nucleus

The low-threshold spike (LTS), generated by the transient Ca(2+) current I(T), plays a pivotal role in thalamic relay cell responsiveness and thus in the nature of the thalamic relay. By injecting depolarizing current ramps at various rates to manipulate the slope of membrane depolarization (dV/dt), we found that an LTS occurred only if dV/dt exceeded a minimum value of approximately 5-12 mV/sec. We injected current ramps of variable dV/dt into relay cells that were sufficiently hyperpolarized to de-inactivate I(T) completely. Higher values of dV/dt activated an LTS. However, lower values of dV/dt eventually led to tonic firing without ever activating an LTS; apparently, the inactivation of I(T) proceeded before I(T) could be recruited. Because the maximum rate of rise of the LTS decreased with slower activating ramps of injected current, we conclude that slower ramps allow increasing inactivation of I(T) before the threshold for its activation gating is reached, and when the injected ramps have a sufficiently low dV/dt, the inactivation is severe enough to prevent activation of an LTS. In the presence of Cs(+), we found that even the lowest dV/dt that we applied led to LTS activation, apparently because Cs(+) reduced the K(+) "leak" conductance and increased neuronal input resistance. Nonetheless, under normal conditions, our data suggest that there is neither significant window current (related to the overlap of the inactivation and activation curves for I(T)), rhythmogenic properties, nor bistability properties for these neurons. Our theoretical results using a minimal model of LTS excitability in these neurons are consistent with the experimental observations and support our conclusions. We suggest that inputs activating very slow EPSPs (i.e., via metabotropic receptors) may be able to inactivate I(T) without generating sizable I(T) and a spurious burst of action potentials to cortex.

High-frequency (300–800 Hz) components in cat geniculate (dLGN) early visual responses

We analysed the early visual responses of relay cells of the dorsal part of cat lateral geniculate nucleus (dLGN) for the occurrence and characteristics of high-frequency (>300 Hz) spike patterns comparable to the high-frequency oscillations (HFO) found in the human somatosensory system. By using a special algorithm for correcting response latency, we can show that the vast majority of dLGN visual responses which were elicited by a sudden change in contrast show HFOs in the range of 300 to more than 800 Hz. After response time correction these HFOs are clearly visible in summed responses, indicating that these patterns are highly reproducible by identical stimuli. On this basis we analysed the HFOs in more detail. We found the oscillation frequency to increase with stimulus contrast and the area of the receptive field centre covered by an excitatory stimulus. Inhibition reduces the oscillation frequency as demonstrated with additional stimulation of the antagonistic surround of the receptive field and by blocking inhibition with micro-iontophoretical application of bicuculline methiodide. The HFO was almost independent of the state of the system as estimated from the EEG pattern. Based on these findings we discuss whether bursts of action potentials triggered by the low-threshold calcium spike (LTS) can contribute to this pattern of visual thalamic activity.

Mathematical models for the spatial receptive-field organization of nonlagged X-cells in dorsal lateral geniculate nucleus of cat.

Spatial receptive fields of relay cells in dorsal lateral geniculate nucleus (dLGN) have commonly been modeled as a difference of two Gaussian functions. We present alternative models for dLGN cells which take known physiological couplings between retina and dLGN and within dLGN into account. The models include excitatory input from a single retinal ganglion cell and feedforward inhibition via intrageniculate interneurons. Mathematical formulas describing the receptive field and response to circular spot stimuli are found both for models with a finite and an infinite number of ganglion-cell inputs to dLGN neurons. The advantage of these models compared to the common difference-of-Gaussians model is that they, in addition to providing mathematical descriptions of the receptive fields of dLGN neurons, also make explicit contributions from the geniculate circuit. Moreover, the model parameters have direct physiological relevance and can be manipulated and measured experimentally. The discrete model is applied to recently published data (Ruksenas et al., 2000) on response versus spot-diameter curves for dLGN cells and for the retinal input to the cell (S-potentials). The models are found to account well for the results for the X-cells in these experiments. Moreover, predictions from the discrete model regarding receptive-field sizes of interneurons, the amount of center-surround antagonism for interneurons compared to relay cells, and distance between neighboring retinal ganglion cells providing input to interneurons, are all compatible with data available in the literature.

Temporal Coding of Visual Information in the Thalamus

The amount of information a sensory neuron carries about a stimulus is directly related to response reliability. We recorded from individual neurons in the cat lateral geniculate nucleus (LGN) while presenting randomly modulated visual stimuli. The responses to repeated stimuli were reproducible, whereas the responses evoked by nonrepeated stimuli drawn from the same ensemble were variable. Stimulus-dependent information was quantified directly from the difference in entropy of these neural responses. We show that a single LGN cell can encode much more visual information than had been demonstrated previously, ranging from 15 to 102 bits/sec across our sample of cells. Information rate was correlated with the firing rate of the cell, for a consistent rate of 3.6 +/- 0.6 bits/spike (mean +/- SD). This information can primarily be attributed to the high temporal precision with which firing probability is modulated; many individual spikes were timed with better than 1 msec precision. We introduce a way to estimate the amount of information encoded in temporal patterns of firing, as distinct from the information in the time varying firing rate at any temporal resolution. Using this method, we find that temporal patterns sometimes introduce redundancy but often encode visual information. The contribution of temporal patterns ranged from -3.4 to +25.5 bits/sec or from -9.4 to +24.9% of the total information content of the responses.