Brain state effects on layer 4 of the awake visual cortex (original) (raw)
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Journal of Neuroscience, 2013
were identified solely by their characteristic response to electrical stimulation of the lateral geniculate nucleus (LGN, 3ϩ spikes at Ͼ600 Hz), and simple cells were identified solely by receptive field structure, requiring spatially separate ON and/or OFF subfields. Notably, no cells met both criteria, and we studied 62 simple cells and 33 SINs. Fourteen cells met neither criterion. These layer 4 populations were markedly distinct. Thus, SINs were far less linear (F1/F0 Ͻ 1), more broadly tuned to stimulus orientation, direction, spatial and temporal frequency, more sensitive to contrast, had much higher spontaneous and stimulus-driven activity, and always had spatially overlapping ON/OFF receptive subfields. SINs responded to drifting gratings with increased firing rates (F0) for all orientations and directions. However, some SINs showed a weaker modulated (F1) response sharply tuned to orientation and/or direction. SINs responded at shorter latencies than simple cells to stationary stimuli, and the responses of both populations could be sustained or transient. Transient simple cells were more sensitive to contrast than sustained simple cells and their visual responses were more frequently suppressed by high contrasts. Finally, cross-correlation between LGN and SIN spike trains confirmed a fast and precisely timed monosynaptic connectivity, supporting the notion that SINs are well suited to provide a fast feedforward inhibition onto targeted cortical populations.
Getting drowsy? Alert/Nonalert transitions and visual thalamocortical network dynamics
2011
The effects of different EEG brain states on spontaneous firing of cortical populations are not well understood. Such state shifts may occur frequently under natural conditions, and baseline firing patterns can impact neural coding (e.g., signal-to-noise ratios, sparseness of coding). Here, we examine the effects of spontaneous transitions from alert to nonalert awake EEG states in the rabbit visual cortex (5 s before and after the state-shifts). In layer 4, we examined putative spiny neurons and fast-spike GABAergic interneurons; in layer 5, we examined corticotectal neurons. We also examined the behavior of retinotopically aligned dorsal lateral geniculate nucleus (LGNd) neurons, usually recorded simultaneously with the above cortical populations. Despite markedly reduced firing and sharply increased bursting in the LGNd neurons following the transition to the nonalert state, little change occurred in the spiny neurons of layer 4. However, fast-spike neurons of layer 4 showed a paradoxical increase in firing rates as thalamic drive decreased in the nonalert state, even though some of these cells received potent monosynaptic input from the same LGNd neurons whose rates were reduced. The firing rates of corticotectal neurons of layer 5, similarly to spiny cells of layer 4, were not state-dependent, but these cells did become more bursty in the nonalert state, as did the fast-spike cells. These results show that spontaneous firing rates of midlayer spiny populations are remarkably conserved following the shift from alert to nonalert states, despite marked reductions in excitatory thalamic drive and increased activity in local fast-spike inhibitory interneurons.
Response variability of neurons in primary visual cortex (V1) of alert monkeys
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1997
Response variability of neurons limits the reliability and resolution of sensory systems. It is generally thought that response variability in the visual system increases at cortical levels, but the causes of the variability have not been identified. We have measured the response variability of neurons in primary visual cortex (V1) of alert monkeys. We recorded from 80 single cells distributed over all V1 layers and from 8 parvocellular cells of the lateral geniculate nucleus. All cells were stimulated with a bar of near-optimal orientation, color, and dimensions while continuously monitoring the eye movements of fixation. To minimize the effects of eye movements, responses that occurred while the eye was relatively steady were selected for analysis. The impulses elicited by each stimulus presentation were counted, and the variance and coefficient of variation were computed. Both measures of response variability were much lower than reported previously for V1 cells of both alert and...
Fast Coding of Orientation in Primary Visual Cortex
PLoS Computational Biology, 2012
Understanding how populations of neurons encode sensory information is a major goal of systems neuroscience. Attempts to answer this question have focused on responses measured over several hundred milliseconds, a duration much longer than that frequently used by animals to make decisions about the environment. How reliably sensory information is encoded on briefer time scales, and how best to extract this information, is unknown. Although it has been proposed that neuronal response latency provides a major cue for fast decisions in the visual system, this hypothesis has not been tested systematically and in a quantitative manner. Here we use a simple 'race to threshold' readout mechanism to quantify the information content of spike time latency of primary visual (V1) cortical cells to stimulus orientation. We find that many V1 cells show pronounced tuning of their spike latency to stimulus orientation and that almost as much information can be extracted from spike latencies as from firing rates measured over much longer durations. To extract this information, stimulus onset must be estimated accurately. We show that the responses of cells with weak tuning of spike latency can provide a reliable onset detector. We find that spike latency information can be pooled from a large neuronal population, provided that the decision threshold is scaled linearly with the population size, yielding a processing time of the order of a few tens of milliseconds. Our results provide a novel mechanism for extracting information from neuronal populations over the very brief time scales in which behavioral judgments must sometimes be made.
Brain state and contrast sensitivity in the awake visual thalamus
Nature Neuroscience, 2006
Neuronal responses to visual stimuli depend on both the nature of the stimulus and brain state. Here we examined the contrast sensitivity of visual thalamic neurons as awake rabbits shifted between alert and nonalert states. We found that despite a large increase in response gain with alertness, contrast sensitivity remained nearly constant. This accurate scaling might be achieved through a balanced increase in excitation and inhibition with alertness.
High Response Reliability of Neurons in Primary Visual Cortex (V1) of Alert, Trained Monkeys
Cerebral Cortex, 2005
The reliability of neuronal responses determines the resources needed to represent the external world and constrains the nature of the neural code. Studies of anesthetized animals have indicated that neuronal responses become progressively more variable as information travels from the retina to the cortex. These results have been interpreted to indicate that perception must be based on pooling across relatively large numbers of cells. However, we find that in alert monkeys, responses in primary visual cortex (V1) are as reliable as the inputs from the retina and the thalamus. Moreover, when the effects of fixational eye movements were minimized, response variability (variance/mean-Fano factor, FF) in all V1 layers was low. When presenting optimal stimuli, the median FF was 0.3. High variability, FF~1, was found only near threshold. Our results suggest that in natural vision, suprathreshold perception can be based on small numbers of optimally stimulated cells.
Inhibition dominates sensory responses in the awake cortex
Nature, 2012
The activity of the cerebral cortex is thought to depend on the precise relationship between synaptic excitation and inhibition 1-4 . In visual cortex, in particular, intracellular measurements have related response selectivity to coordinated increases in excitation and inhibition 5-9 . These measurements, however, have all been performed during anaesthesia, which strongly influences cortical state 10 and therefore sensory processing 7,11-15 . The synaptic activity evoked by visual stimulation during wakefulness is unknown. Here, we measured visually evoked responses -and the underlying synaptic conductances -in the visual cortex of anaesthetised and awake mice. Under anaesthesia, responses could be elicited from a large region of visual space 16 and were prolonged in time. During wakefulness responses were more spatially selective and much briefer. Whole-cell patch-clamp recordings of synaptic conductances 5,17 revealed a surprising difference in synaptic inhibition during the two conditions. Whereas under anaesthesia inhibition tracked excitation in amplitude and spatial selectivity, during wakefulness it was much stronger than excitation and exhibited extremely broad spatial selectivity. We conclude that during wakefulness cortical responses to visual stimulation are dominated by synaptic inhibition, restricting their spatial spread and temporal persistence. These results provide the first direct glimpse of synaptic mechanisms that control visual responses in the awake cortex.
The linearity and selectivity of neuronal responses in awake visual cortex
Journal of Vision, 2009
Neurons in primary visual cortex (V1) are frequently classified based on their response linearity: the extent in which their visual responses to drifting gratings resemble a linear replica of the stimulus. This classification is supported by the finding that response linearity is bimodally distributed across neurons in area V1 of anesthetized animals. However, recent studies suggest that such bimodal distribution may not reflect two neuronal types but a nonlinear relationship between the membrane potential and the spike output. A main limitation of these previous studies is that they measured response linearity in anesthetized animals, where the distance between the neuronal membrane potential and spike threshold is artificially increased by anesthesia. Here, we measured V1 response linearity in the awake brain and its correlation with the neuronal spontaneous firing rate, which is related to the distance between membrane potential and threshold. Our results demonstrate that response linearity is bimodally distributed in awake V1 but that it is poorly correlated with spontaneous firing rate. In contrast, the spontaneous firing rate is best correlated to the response selectivity and response latency to stimuli.
Feature selectivity is stable in primary visual cortex across a range of spatial frequencies
Scientific Reports, 2018
Reliable perception of environmental signals is a critical first step to generating appropriate responses and actions in awake behaving animals. The extent to which stimulus features are stably represented at the level of individual neurons is not well understood. To address this issue, we investigated the persistence of stimulus response tuning over the course of 1–2 weeks in the primary visual cortex of awake, adult mice. Using 2-photon calcium imaging, we directly compared tuning stability to two stimulus features (orientation and spatial frequency) within the same neurons, specifically in layer 2/3 excitatory neurons. The majority of neurons that were tracked and tuned on consecutive imaging sessions maintained stable orientation and spatial frequency preferences (83% and 76% of the population, respectively) over a 2-week period. Selectivity, measured as orientation and spatial frequency bandwidth, was also stable. Taking into account all 4 parameters, we found that the proporti...