Neurons In Lateral Geniculate Nucleus Research Articles

Suppression of V1 Feedback Produces a Shift in the Topographic Representation of Receptive Fields of LGN Cells by Unmasking Latent Retinal Drives.

In awake monkeys, we used repetitive transcranial magnetic stimulation (rTMS) to focally inactivate visual cortex while measuring the responsiveness of parvocellular lateral geniculate nucleus (LGN) neurons. Effects were noted in 64/75 neurons, and could be divided into 2 main groups: (1) for 39 neurons, visual responsiveness decreased and visual latency increased without apparent shift in receptive field (RF) position and (2) a second group (n = 25, 33% of the recorded cells) whose excitability was not compromised, but whose RF position shifted an average of 4.5°. This change is related to the retinotopic correspondence observed between the recorded thalamic area and the affected cortical zone. The effect of inactivation for this group of neurons was compatible with silencing the original retinal drive and unmasking a second latent retinal drive onto the studied neuron. These results indicate novel and remarkable dynamics in thalamocortical circuitry that force us to reassess constraints on retinogeniculate transmission.

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus

Extraclassical surround suppression is a prominent receptive field property of neurons in the lateral geniculate nucleus (LGN) of the dorsal thalamus, influencing stimulus size tuning, response gain control, and temporal features of visual responses. Despite evidence for the involvement of both retinal and nonretinal circuits in the generation of extraclassical suppression, we lack an understanding of the relative roles played by these pathways and how they interact during visual stimulation. To determine the contribution of retinal and nonretinal mechanisms to extraclassical suppression in the feline, we made simultaneous single-unit recordings from synaptically connected retinal ganglion cells and LGN neurons and measured the influence of stimulus size on the spiking activity of presynaptic and postsynaptic neurons. Results show that extraclassical suppression is significantly stronger for LGN neurons than for their retinal inputs, indicating a role for extraretinal mechanisms. Further analysis revealed that the enhanced suppression can be accounted for by mechanisms that suppress the effectiveness of retinal inputs in evoking LGN spikes. Finally, an examination of the time course for the onset of extraclassical suppression in the LGN and the size-dependent modulation of retinal spike efficacy suggests the early phase of augmented suppression involves local thalamic circuits. Together, these results demonstrate that the LGN is much more than a simple relay for retinal signals to cortex; it also filters retinal spikes dynamically on the basis of stimulus statistics to adjust the gain of visual signals delivered to cortex. <b>SIGNIFICANCE STATEMENT</b> The lateral geniculate nucleus (LGN) is the gateway through which retinal information reaches the cerebral cortex. Within the LGN, neuronal responses are often suppressed by stimuli that extend beyond the classical receptive field. This form of suppression, called extraclassical suppression, serves to adjust the size tuning, response gain, and temporal response properties of neurons. Given the important influence of extraclassical suppression on visual signals delivered to cortex, we performed experiments to determine the circuit mechanisms that contribute to extraclassical suppression in the LGN. Results show that suppression is augmented beyond that provided by direct retinal inputs and delayed, consistent with polysynaptic inhibition. Importantly, these mechanisms influence the effectiveness of incoming retinal signals, thereby filtering the signals ultimately conveyed to cortex.

A developmental study of glutamatergic neuron populations in the ventrobasal and the lateral geniculate nucleus of the thalamus: Comparing Genetic Absence Rats from Strasbourg (GAERS) and normal control wistar rats

An imbalance of GABAergic inhibition and glutamatergic excitation is suspected to be the cause of absence epileptic seizures. Absence seizures are known to be generated in thalamocortical circuitry. In the present study we used light microscopy immunohistochemistry to quantify the density of glutamate+ve neurons at two developmental stages (P10 and P60) in two thalamic nuclei, the ventrobasal (VB) and lateral geniculate nucleus (LGN) in Wistar rats and compared the results with similar data obtained from genetic absence epilepsy rats from Strasbourg (GAERS).Rats were perfused transcardially with glutaraldehyde and paraformaldehyde fixative, then samples from VB and LGN were removed from each animal and sectioned. The glutamatergic neurons were labelled using light-microscopic glutamate immunohistochemistry. The disector method was used to quantify the glutamate+ve neurons in VB and LGN of GAERS and Wistar rats. The data were statistically analyzed.The distribution of the glutamate+ve neurons in the VB thalamic nucleus showed a significant reduction in the neuronal profiles per unit thalamic area from P10 to P60 in both Wistar and GAERS. The decrease was greater in the GAERS compared to the Wistar animals. However, in the LGN no reduction was observed either in the Wistar or in the GAERS. Comparing the density of glutamate+ve neurons in the VB thalamic nucleus of P10 of Wistar animals with of P10 GAERS showed statistically significant greater densities of these neurons in GAERS than in the Wistar rats. However no significant difference was present at P60 between the Wistar and GAERS animals.The disproportional decrease in GAERS may be related to the onset of absence seizures or may be related to neurogenesis of absence epilepsy.

Retinal and Nonretinal Contributions to Extraclassical Surround Suppression in the Lateral Geniculate Nucleus.

The lateral geniculate nucleus (LGN) is the gateway through which retinal information reaches the cerebral cortex. Within the LGN, neuronal responses are often suppressed by stimuli that extend beyond the classical receptive field. This form of suppression, called extraclassical suppression, serves to adjust the size tuning, response gain, and temporal response properties of neurons. Given the important influence of extraclassical suppression on visual signals delivered to cortex, we performed experiments to determine the circuit mechanisms that contribute to extraclassical suppression in the LGN. Results show that suppression is augmented beyond that provided by direct retinal inputs and delayed, consistent with polysynaptic inhibition. Importantly, these mechanisms influence the effectiveness of incoming retinal signals, thereby filtering the signals ultimately conveyed to cortex.

Tuning electrical stimulation for thalamic visual prosthesis: An autoencoder-based approach.

Visual prosthesis holds hope of vision restoration for millions with retinal degenerative diseases. Machine learning techniques such as artificial neural networks could help in improving prosthetic devices as they could learn how the brain encodes information and imitate that code. This paper introduces an autoencoder-based approach for tuning thalamic visual prostheses. The objective of the proposed approach is to estimate electrical stimuli that are equivalent to a given natural visual stimulus, in a way such that they both elicit responses that are as similar as possible when introduced to a Lateral Geniculate Nucleus (LGN) population. Applying the proposed method to a probabilistic model of LGN neurons, results demonstrate a significant similarity between both responses with a mean correlation of 0.672 for optimal electrodes placement and 0.354 for random electrodes placement. The results indicate the efficacy of the proposed approach in estimating an electrical stimulus equivalent to a specific visual stimulus.

Nonlinear computations shaping temporal processing of precortical vision.

Computations performed by the visual pathway are constructed by neural circuits distributed over multiple stages of processing, and thus it is challenging to determine how different stages contribute on the basis of recordings from single areas. In the current article, we address this problem in the lateral geniculate nucleus (LGN), using experiments combined with nonlinear modeling capable of isolating various circuit contributions. We recorded cat LGN neurons presented with temporally modulated spots of various sizes, which drove temporally precise LGN responses. We utilized simultaneously recorded S-potentials, corresponding to the primary retinal ganglion cell (RGC) input to each LGN cell, to distinguish the computations underlying temporal precision in the retina from those in the LGN. Nonlinear models with excitatory and delayed suppressive terms were sufficient to explain temporal precision in the LGN, and we found that models of the S-potentials were nearly identical, although with a lower threshold. To determine whether additional influences shaped the response at the level of the LGN, we extended this model to use the S-potential input in combination with stimulus-driven terms to predict the LGN response. We found that the S-potential input "explained away" the major excitatory and delayed suppressive terms responsible for temporal patterning of LGN spike trains but revealed additional contributions, largely PULL suppression, to the LGN response. Using this novel combination of recordings and modeling, we were thus able to dissect multiple circuit contributions to LGN temporal responses across retina and LGN, and set the foundation for targeted study of each stage.

Thalamic Visual Prosthesis.

Glaucoma is a neurological disorder leading to blindness initially through the loss of retinal ganglion cells, followed by loss of neurons higher in the visual system. Some work has been undertaken to develop prostheses for glaucoma patients targeting tissues along the visual pathway, including the lateral geniculate nucleus (LGN) of the thalamus, but especially the visual cortex. This review makes the case for a visual prosthesis that targets the LGN. The compact nature and orderly structure of this nucleus make it a potentially better target to restore vision than the visual cortex. Existing research for the development of a thalamic visual prosthesis will be discussed along with the gaps that need to be addressed before such a technology could be applied clinically, as well as the challenge posed by the loss of LGN neurons as glaucoma progresses.

Temporal and spatial tuning of dorsal lateral geniculate nucleus neurons in unanesthetized rats.

Visual response properties of neurons in the dorsolateral geniculate nucleus (dLGN) have been well described in several species, but not in rats. Analysis of responses from the unanesthetized rat dLGN will be needed to develop quantitative models that account for visual behavior of rats. We recorded visual responses from 130 single units in the dLGN of 7 unanesthetized rats. We report the response amplitudes, temporal frequency, and spatial frequency sensitivities in this population of cells. In response to 2-Hz visual stimulation, dLGN cells fired 15.9 ± 11.4 spikes/s (mean ± SD) modulated by 10.7 ± 8.4 spikes/s about the mean. The optimal temporal frequency for full-field stimulation ranged from 5.8 to 19.6 Hz across cells. The temporal high-frequency cutoff ranged from 11.7 to 33.6 Hz. Some cells responded best to low temporal frequency stimulation (low pass), and others were strictly bandpass; most cells fell between these extremes. At 2- to 4-Hz temporal modulation, the spatial frequency of drifting grating that drove cells best ranged from 0.008 to 0.18 cycles per degree (cpd) across cells. The high-frequency cutoff ranged from 0.01 to 1.07 cpd across cells. The majority of cells were driven best by the lowest spatial frequency tested, but many were partially or strictly bandpass. We conclude that single units in the rat dLGN can respond vigorously to temporal modulation up to at least 30 Hz and spatial detail up to 1 cpd. Tuning properties were heterogeneous, but each fell along a continuum; we found no obvious clustering into discrete cell types along these dimensions.

Stimulus Contrast and Retinogeniculate Signal Processing

Neuronal signals conveying luminance contrast play a key role in nearly all aspects of perception, including depth perception, texture discrimination, and motion perception. Although much is known about the retinal mechanisms responsible for encoding contrast information, relatively little is known about the relationship between stimulus contrast and the processing of neuronal signals between visual structures. Here, we describe simultaneous recordings from monosynaptically connected retinal ganglion cells and lateral geniculate nucleus (LGN) neurons in the cat to determine how stimulus contrast affects the communication of visual signals between the two structures. Our results indicate that: (1) LGN neurons typically reach their half-maximal response at lower contrasts than their individual retinal inputs and (2) LGN neurons exhibit greater contrast-dependent phase advance (CDPA) than their retinal inputs. Further analyses suggests that increased sensitivity relies on spatial convergence of multiple retinal inputs, while increased CDPA is achieved, in part, on temporal summation of arriving signals.

Visual Receptive Field Properties of Neurons in the Mouse Lateral Geniculate Nucleus.

The lateral geniculate nucleus (LGN) is increasingly regarded as a “smart-gating” operator for processing visual information. Therefore, characterizing the response properties of LGN neurons will enable us to better understand how neurons encode and transfer visual signals. Efforts have been devoted to study its anatomical and functional features, and recent advances have highlighted the existence in rodents of complex features such as direction/orientation selectivity. However, unlike well-researched higher-order mammals such as primates, the full array of response characteristics vis-à-vis its morphological features have remained relatively unexplored in the mouse LGN. To address the issue, we recorded from mouse LGN neurons using multisite-electrode-arrays (MEAs) and analysed their discharge patterns in relation to their location under a series of visual stimulation paradigms. Several response properties paralleled results from earlier studies in the field and these include centre-surround organization, size of receptive field, spontaneous firing rate and linearity of spatial summation. However, our results also revealed “high-pass” and “low-pass” features in the temporal frequency tuning of some cells, and greater average contrast gain than reported by earlier studies. In addition, a small proportion of cells had direction/orientation selectivity. Both “high-pass” and “low-pass” cells, as well as direction and orientation selective cells, were found only in small numbers, supporting the notion that these properties emerge in the cortex. ON- and OFF-cells showed distinct contrast sensitivity and temporal frequency tuning properties, suggesting parallel projections from the retina. Incorporating a novel histological technique, we created a 3-D LGN volume model explicitly capturing the morphological features of mouse LGN and localising individual cells into anterior/middle/posterior LGN. Based on this categorization, we show that the ON/OFF, DS/OS and linear response properties are not regionally restricted. Our study confirms earlier findings of spatial pattern selectivity in the LGN, and builds on it to demonstrate that relatively elaborate features are computed early in the visual pathway.

The multifunctional lateral geniculate nucleus.

Providing the critical link between the retina and visual cortex, the well-studied lateral geniculate nucleus (LGN) has stood out as a structure in search of a function exceeding the mundane 'relay'. For many mammals, it is structurally impressive: Exquisite lamination, sophisticated microcircuits, and blending of multiple inputs suggest some fundamental transform. This impression is bolstered by the fact that numerically, the retina accounts for a small fraction of its input. Despite such promise, the extent to which an LGN neuron separates itself from its retinal brethren has proven difficult to appreciate. Here, I argue that whereas retinogeniculate coupling is strong, what occurs in the LGN is judicious pruning of a retinal drive by nonretinal inputs. These nonretinal inputs reshape a receptive field that under the right conditions departs significantly from its retinal drive, even if transiently. I first review design features of the LGN and follow with evidence for 10 putative functions. Only two of these tend to surface in textbooks: parsing retinal axons by eye and functional group and gating by state. Among the remaining putative functions, implementation of the principle of graceful degradation and temporal decorrelation are at least as interesting but much less promoted. The retina solves formidable problems imposed by physics to yield multiple efficient and sensitive representations of the world. The LGN applies context, increasing content, and gates several of these representations. Even if the basic concentric receptive field remains, information transmitted for each LGN spike relative to each retinal spike is measurably increased.

Visual evoked potentials of Niemann-Pick type C1 mice reveal an impairment of the visual pathway that is rescued by 2-hydroxypropyl-ß-cyclodextrin.

BackgroundThe lysosomal storage disorder, Niemann Pick type C1 (NPC1), presents a variable phenotype including neurovisceral and neurological symptoms. 2-Hydroxypropyl-ß-cyclodextrin (HPßCD)-based therapies are presently the most promising route of intervention. While severe cerebellar dysfunction remains the main disabling feature of NPC1, sensory functions including auditory and olfactory ones are also affected. Morphological and functional anomalies of Npc1−/− mouse retina have also been observed, although the functional integrity of the visual pathway from retina to visual cortex is still unsettled. We have addressed this issue by characterizing the visual evoked potential (VEP) response of Npc1−/− mice and determining if/how HPßCD administration influences the VEPs of both Npc1−/− and Npc1+/+ mice.MethodsVEP elicited by a brief visual stimulus were recorded from the scalp overlying the visual cortex of adult (PN, postnatal days 60, 75, 85 and 100) Npc1+/+ and Npc1−/− mice that had received repeated injections of either HPßCD or plain vehicle. The first injection was given at PN4 and was followed by a second one at PN7 and thereafter by weekly injections up to PN49. Cholesterol accumulation and myelin loss were finally assessed by filipin staining and myelin basic protein immunohistochemistry, respectively.Results and discussionWe have found that the transmission of visual signals from retina to visual cortex is negatively influenced by the loss of Npc1 function. In fact, the VEP response of Npc1−/− mice displayed a highly significant increase in the latency compared to that of Npc1+/+ mice. HPßCD administration fully rescued this defect and counteracted the cholesterol accumulation in retinal ganglion cells and dorsal lateral geniculate nucleus neurons, as well as the myelin loss in optic nerve fibers and axons projecting to the visual cortex observed in of Npc1−/− mice. By contrast, HPßCD administration had no effect on the VEP response of Npc1+/+ mice, further strengthening the treatment efficacy.ConclusionsThis study pinpoints the analysis of VEP response as a potentially accurate and non-invasive approach to assess neural activity and visual information processing in NPC1 patients, as well as for monitoring the progression of the disease and assessing the efficacy of potential therapies.Electronic supplementary materialThe online version of this article (doi:10.1186/s13023-015-0348-0) contains supplementary material, which is available to authorized users.

A computational relationship between thalamic sensory neural responses and contrast perception.

Uncovering the relationship between sensory neural responses and perceptual decisions remains a fundamental problem in neuroscience. Decades of experimental and modeling work in the sensory cortex have demonstrated that a perceptual decision pool is usually composed of tens to hundreds of neurons, the responses of which are significantly correlated not only with each other, but also with the behavioral choices of an animal. Few studies, however, have measured neural activity in the sensory thalamus of awake, behaving animals. Therefore, it remains unclear how many thalamic neurons are recruited and how the information from these neurons is pooled at subsequent cortical stages to form a perceptual decision. In a previous study we measured neural activity in the macaque lateral geniculate nucleus (LGN) during a two alternative forced choice (2AFC) contrast detection task, and found that single LGN neurons were significantly correlated with the monkeys’ behavioral choices, despite their relatively poor contrast sensitivity and a lack of overall interneuronal correlations. We have now computationally tested a number of specific hypotheses relating these measured LGN neural responses to the contrast detection behavior of the animals. We modeled the perceptual decisions with different numbers of neurons and using a variety of pooling/readout strategies, and found that the most successful model consisted of about 50–200 LGN neurons, with individual neurons weighted differentially according to their signal-to-noise ratios (quantified as d-primes). These results supported the hypothesis that in contrast detection the perceptual decision pool consists of multiple thalamic neurons, and that the response fluctuations in these neurons can influence contrast perception, with the more sensitive thalamic neurons likely to exert a greater influence.

Functions of synapsins in corticothalamic facilitation: important roles of synapsin I.

The synaptic vesicle associated proteins synapsin I and synapsin II have important functions in synaptic short-term plasticity. We investigated their functions in cortical facilitatory feedback to neurons in dorsal lateral geniculate nucleus (dLGN), feedback that has important functions in state-dependent regulation of thalamic transmission of visual input to cortex. We compared results from normal wild-type (WT) mice and synapsin knockout (KO) mice in several types of synaptic plasticity, and found clear differences between the responses of neurons in the synapsin I KO and the WT, but no significant differences between the synapsin II KO and the WT. These results are in contrast to the important role of synapsin II previously demonstrated in similar types of synaptic plasticity in other brain regions, indicating that the synapsins can have different roles in similar types of STP in different parts of the brain. The synaptic vesicle associated proteins synapsin I (SynI) and synapsin II (SynII) have important functions in several types of synaptic short-term plasticity in the brain, but their separate functions in different types of synapses are not well known. We investigated possible distinct functions of the two synapsins in synaptic short-term plasticity at corticothalamic synapses on relay neurons in the dorsal lateral geniculate nucleus. These synapses provide excitatory feedback from visual cortex to the relay cells, feedback that can facilitate transmission of signals from retina to cortex. We compared results from normal wild-type (WT), SynI knockout (KO) and SynII KO mice, in three types of synaptic plasticity mainly linked to presynaptic mechanism. In SynI KO mice, paired-pulse stimulation elicited increased facilitation at short interpulse intervals compared to the WT. Pulse-train stimulation elicited weaker facilitation than in the WT, and also post-tetanic potentiation was weaker in SynI KO than in the WT. Between SynII KO and the WT we found no significant differences. Thus, SynI has important functions in these types of synaptic plasticity at corticothalamic synapses. Interestingly, our data are in contrast to the important role of SynII previously shown for sustained synaptic transmission during intense stimulation in excitatory synapses in other parts of the brain, and our results suggest that SynI and SynII may have different roles in similar types of STP in different parts of the brain.

Contrast invariance of orientation tuning in the lateral geniculate nucleus of the feline visual system.

Responses of most neurons in the primary visual cortex of mammals are markedly selective for stimulus orientation and their orientation tuning does not vary with changes in stimulus contrast. The basis of such contrast invariance of orientation tuning has been shown to be the higher variability in the response for low-contrast stimuli. Neurons in the lateral geniculate nucleus (LGN), which provides the major visual input to the cortex, have also been shown to have higher variability in their response to low-contrast stimuli. Parallel studies have also long established mild degrees of orientation selectivity in LGN and retinal cells. In our study, we show that contrast invariance of orientation tuning is already present in the LGN. In addition, we show that the variability of spike responses of LGN neurons increases at lower stimulus contrasts, especially for non-preferred orientations. We suggest that such contrast- and orientation-sensitive variability not only explains the contrast invariance observed in the LGN but can also underlie the contrast-invariant orientation tuning seen at the level of the primary visual cortex.

Hour-long adaptation in the awake early visual system.

Sensory adaptation serves to adjust awake brains to changing environments on different time scales. However, adaptation has been studied traditionally under anesthesia and for short time periods. Here, we demonstrate in awake rabbits a novel type of sensory adaptation that persists for >1 h and acts on visual thalamocortical neurons and their synapses in the input layers of the visual cortex. Following prolonged visual stimulation (10-30 min), cells in the dorsal lateral geniculate nucleus (LGN) show a severe and prolonged reduction in spontaneous firing rate. This effect is bidirectional, and prolonged visually induced response suppression is followed by a prolonged increase in spontaneous activity. The reduction in thalamic spontaneous activity following prolonged visual activation is accompanied by increases in 1) response reliability, 2) signal detectability, and 3) the ratio of visual signal/spontaneous activity. In addition, following such prolonged activation of an LGN neuron, the monosynaptic currents generated by thalamic impulses in layer 4 of the primary visual cortex are enhanced. These results demonstrate that in awake brains, prolonged sensory stimulation can have a profound, long-lasting effect on the information conveyed by thalamocortical inputs to the visual cortex.

Perceptual decision related activity in the lateral geniculate nucleus.

Fundamental to neuroscience is the understanding of how the language of neurons relates to behavior. In the lateral geniculate nucleus (LGN), cells show distinct properties such as selectivity for particular wavelengths, increments or decrements in contrast, or preference for fine detail versus rapid motion. No studies, however, have measured how LGN cells respond when an animal is challenged to make a perceptual decision using information within the receptive fields of those LGN cells. In this study we measured neural activity in the macaque LGN during a two-alternative, forced-choice (2AFC) contrast detection task or during a passive fixation task and found that a small proportion (13.5%) of single LGN parvocellular (P) and magnocellular (M) neurons matched the psychophysical performance of the monkey. The majority of LGN neurons measured in both tasks were not as sensitive as the monkey. The covariation between neural response and behavior (quantified as choice probability) was significantly above chance during active detection, even when there was no external stimulus. Interneuronal correlations and task-related gain modulations were negligible under the same condition. A bottom-up pooling model that used sensory neural responses to compute perceptual choices in the absence of interneuronal correlations could fully explain these results at the level of the LGN, supporting the hypothesis that the perceptual decision pool consists of multiple sensory neurons and that response fluctuations in these neurons can influence perception.

Weak orientation and direction selectivity in lateral geniculate nucleus representing central vision in the gray squirrel Sciurus carolinensis.

Classic studies of lateral geniculate nucleus (LGN) and visual cortex (V1) in carnivores and primates have found that a majority of neurons in LGN exhibit a center-surround organization, while V1 neurons exhibit strong orientation selectivity and, in many species, direction selectivity. Recent work in the mouse and the monkey has discovered previously unknown classes of orientation- and direction-selective neurons in LGN. Furthermore, some recent studies in the mouse report that many LGN cells exhibit pronounced orientation biases that are of comparable strength to the subthreshold inputs to V1 neurons. These results raise the possibility that, in rodents, orientation biases of individual LGN cells make a substantial contribution to cortical orientation selectivity. Alternatively, the size and contribution of orientation- or direction-selective channels from LGN to V1 may vary across mammals. To address this question, we examined orientation and direction selectivity in LGN and V1 neurons of a highly visual diurnal rodent: the gray squirrel. In the representation of central vision, only a few LGN neurons exhibited strong orientation or direction selectivity. Across the population, LGN neurons showed weak orientation biases and were much less selective for orientation compared with V1 neurons. Although direction selectivity was weak overall, LGN layers 3abc, which contain neurons that express calbindin, exhibited elevated direction selectivity index values compared with LGN layers 1 and 2. These results suggest that, for central visual fields, the contribution of orientation- and direction-selective channels from the LGN to V1 is small in the squirrel. As in other mammals, this small contribution is elevated in the calbindin-positive layers of the LGN.

Surround suppression and temporal processing of visual signals.

Extraclassical surround suppression strongly modulates responses of neurons in the retina, lateral geniculate nucleus (LGN), and primary visual cortex. Although a great deal is known about the spatial properties of extraclassical suppression and the role it serves in stimulus size tuning, relatively little is known about how extraclassical suppression shapes visual processing in the temporal domain. We recorded the spiking activity of retinal ganglion cells and LGN neurons in the cat to test the hypothesis that extraclassical suppression influences temporal features of visual responses in the early visual system. Our results demonstrate that extraclassical suppression not only shifts the distribution of interspike intervals in a manner that decreases the efficacy of neuronal communication, it also decreases the reliability of neuronal responses to visual stimuli and it decreases the duration of visual responses, an effect that underlies a rightward shift in the temporal frequency tuning of LGN neurons. Taken together, these results reveal a dynamic relationship between extraclassical suppression and the temporal features of neuronal responses.

T-type calcium channels promote predictive homeostasis of input-output relations in thalamocortical neurons of lateral geniculate nucleus.

A general theory views the function of all neurons as prediction, and one component of this theory is that of “predictive homeostasis” or “prediction error.” It is well established that sensory systems adapt so that neuronal output maintains sensitivity to sensory input, in accord with information theory. Predictive homeostasis applies the same principle at the cellular level, where the challenge is to maintain membrane excitability at the optimal homeostatic level so that spike generation is maximally sensitive to small gradations in synaptic drive. Negative feedback is a hallmark of homeostatic mechanisms, as exemplified by depolarization-activated potassium channels. In contrast, T-type calcium channels exhibit positive feedback that appears at odds with the theory. In thalamocortical neurons of lateral geniculate nucleus (LGN), T-type channels are capable of causing bursts of spikes with an all-or-none character in response to excitation from a hyperpolarized potential. This “burst mode” would partially uncouple visual input from spike output and reduce the information spikes convey about gradations in visual input. However, past observations of T-type-driven bursts may have resulted from unnaturally high membrane excitability. Here we have mimicked within rat brain slices the patterns of synaptic conductance that occur naturally during vision. In support of the theory of predictive homeostasis, we found that T-type channels restored excitability toward its homeostatic level during periods of hyperpolarization. Thus, activation of T-type channels allowed two retinal input spikes to cause one output spike on average, and we observed almost no instances in which output count exceeded input count (a “burst”). T-type calcium channels therefore help to maintain a single optimal mode of transmission rather than creating a second mode. More fundamentally our results support the general theory, which seeks to predict the properties of a neuron's ion channels and synapses given knowledge of natural patterns of synaptic input.