Dose-dependent changes in orientation amplitude maps in the cat visual cortex after propofol bolus injections.

A general intravenous anesthetic propofol (2,6-diisopropylphenol) is widely used in clinical, veterinary practice and animal experiments. It activates gamma- aminobutyric acid (GABAa) receptors. Though the cerebral cortex is one of the major targets of propofol action, no study of dose dependency of propofol action on cat visual cortex was performed yet. Also, no such investigation was done until now using intrinsic signal optical imaging. Here, we report for the first time on the dependency of optical signal in the visual cortex (area 17/area 18) on the propofol dose. Optical imaging of intrinsic responses to visual stimuli was performed in cats before and after propofol bolus injections at different doses on the background of continuous propofol infusion. Orientation amplitude maps were recorded. We found that amplitude of optical signal significantly decreased after a bolus dose of propofol. The effect was dose- and time-dependent producing stronger suppression of optical signal under the highest bolus propofol doses and short time interval after injection. In each hemisphere, amplitude at cardinal and oblique orientations decreased almost equally. However, surprisingly, amplitude at cardinal orientations in the ipsilateral hemisphere was depressed stronger than in contralateral cortex at most time intervals. As the magnitude of optical signal represents the strength of orientation tuned component, these our data give new insights on the mechanisms of generation of orientation selectivity. Our results also provide new data toward understanding brain dynamics under anesthesia and suggest a recommendation for conducting intrinsic signal optical imaging experiments on cortical functioning under propofol anesthesia.

Adaptive behavior of neighboring neurons during adaptation-induced plasticity of orientation tuning in VI.

BACKGROUND: Sensory neurons display transient changes of their response properties following prolonged exposure to an appropriate stimulus (adaptation). In adult cat primary visual cortex, orientation-selective neurons shift their preferred orientation after being adapted to a non-preferred orientation. The direction of those shifts, towards (attractive) or away (repulsive) from the adapter depends mostly on adaptation duration. How the adaptive behavior of a neuron is related to that of its neighbors remains unclear. RESULTS: Here we show that in most cases (75%), cells shift their preferred orientation in the same direction as their neighbors. We also found that cells shifting preferred orientation differently from their neighbors (25%) display three interesting properties: (i) larger variance of absolute shift amplitude, (ii) wider tuning bandwidth and (iii) larger range of preferred orientations among the cluster of cells. Several response properties of V1 neurons depend on their location within the cortical orientation map. Our results suggest that recording sites with both attractive and repulsive shifts following adaptation may be located in close proximity to iso-orientation domain boundaries or pinwheel centers. Indeed, those regions have a more diverse orientation distribution of local inputs that could account for the three properties above. On the other hand, sites with all cells shifting their preferred orientation in the same direction could be located within iso-orientation domains. CONCLUSIONS: Our results suggest that the direction and amplitude of orientation preference shifts in V1 depend on location within the orientation map. This anisotropy of adaptation-induced plasticity, comparable to that of the visual cortex itself, could have important implications for our understanding of visual adaptation at the psychophysical level.

Synchrony between orientation-selective neurons is modulated during adaptation-induced plasticity in cat visual cortex.

BACKGROUND: Visual neurons respond essentially to luminance variations occurring within their receptive fields. In primary visual cortex, each neuron is a filter for stimulus features such as orientation, motion direction and velocity, with the appropriate combination of features eliciting maximal firing rate. Temporal correlation of spike trains was proposed as a potential code for linking the neuronal responses evoked by various features of a same object. In the present study, synchrony strength was measured between cells following an adaptation protocol (prolonged exposure to a non-preferred stimulus) which induce plasticity of neurons' orientation preference. RESULTS: Multi-unit activity from area 17 of anesthetized adult cats was recorded. Single cells were sorted out and (1) orientation tuning curves were measured before and following 12 min adaptation and 60 min after adaptation (2) pairwise synchrony was measured by an index that was normalized in relation to the cells' firing rate. We first observed that the prolonged presentation of a non-preferred stimulus produces attractive (58%) and repulsive (42%) shifts of cell's tuning curves. It follows that the adaptation-induced plasticity leads to changes in preferred orientation difference, i.e. increase or decrease in tuning properties between neurons. We report here that, after adaptation, the neuron pairs that shared closer tuning properties display a significant increase of synchronization. Recovery from adaptation was accompanied by a return to the initial synchrony level. CONCLUSION: We conclude that synchrony reflects the similarity in neurons' response properties, and varies accordingly when these properties change.

Spatial frequency characteristics of nearby neurons in cats' visual cortex.

Various methods have allowed mapping of responses to several stimulus features on the cortical surface, particularly edge orientation and motion direction. The cortical mapping of spatial frequencies (SF), which is the basic property that leads to perception of spatial details of visual objects, is still controversial. We recorded simultaneously extracellular action potentials from neighboring cells in superficial layers of the area 17-18 border region of anesthetized cats. Responses of nearby cells to sine-wave gratings of varying SF were analyzed. Spatial frequency tuning curves were cross-correlated to establish the degree of similarity between the curves and optimal SFs were compared for each pair of neurons. The investigation showed that only about a half of nearby neurons exhibited close optimal SFs and similar tuning curves. The results suggest that SF channels do not show a clear clustering within a small pool of neurons. Such organization may contribute to the perception of spatial details at all orientations and motion directions.

Neuron participation in a synchrony-encoding assembly.

BACKGROUND: Synchronization of action potentials between neurons is considered to be an encoding process that allows the grouping of various and multiple features of an image leading to a coherent perception. How this coding neuronal assembly is configured is debated. We have previously shown that the magnitude of synchronization between excited neurons is stimulus-dependent. In the present investigation we compare the levels of synchronization between synchronizing individual neurons and the synchronizing pool of cells to which they belong. RESULTS: Even though neurons belonged to their respective pools, some cells synchronized for all presented stimuli while others were rather selective and only a few stimulating conditions produced a significant synchronization. In addition the experiments show that one synchronizing pair rarely replicates the level of synchrony between corresponding groups of units. But when synchronizing clusters of neurons increase in number, the correlation (measured as a coefficient of determination) between unit synchronization and the synchronization between the entire pools of cells to which individual neurons belong improves. CONCLUSION: These results prompt the hypothesis that random or spontaneous synchronization becomes progressively less important, whereas coincident spikes related to encoding properties of targets gain significance because a particular configuration of an image biases the excitatory inputs in favor of connections driven by the applied features of the stimulus.

Influence of NO downregulation on oscillatory evoked responses in developing rat superior colliculus.

Nitric oxide (NO) is involved in neuronal transmission by modulating neurotransmitter release in adults and in stabilizing synaptic connections in developing brains. We investigated the influence of downregulation of NO synthesis on oscillatory components of ON and OFF evoked field potentials in the rat superior colliculus. NO synthesis was decreased by inhibiting nitric oxide synthase (NOS) with an acute microinjection of N(omega)-nitro-L-arginine methyl ester (L-NAME). The study focuses on rhythmic activity by analyzing fast Fourier transform (FFT). Collicular responses were recorded in anesthetized rats, at postnatal days (PND) 13-19 and adults. This time window was chosen because it is centered on eye opening. NO downregulation resulted in a dual effect depending on age and response-type. NO synthesis inhibition decreased the magnitude of oscillations in ON responses in the youngest animals (PND13-14), whereas oscillations of frequencies higher than 20 Hz in OFF responses were increased in all age groups of developing rats. In adults NO downregulation increased oscillations in ON responses and decreased oscillations in OFF responses. L-Arginine was used to increase NOS activity and its injection produced effects opposite to those seen with L-NAME. Slow oscillatory components (7-12 Hz) were unaffected in all experiments. Our data together with results reported in the literature suggest that rhythmic patterns of activity are NO-dependent.

Analysis of frequency components of cortical potentials evoked by progressive misalignment of Kanizsa squares.

Cortical gamma oscillations (20-100 Hz) are thought to play an important role in encoding visual perception. If so they should emerge at about threshold. In the present investigation we examined the latter proposal. Visual responses were recorded in occipital, temporal and parietal areas (stimulus duration 512 ms). Oscillation strength and frequency were derived from FFT analysis and wavelet transforms. The specific goals of the present study are: 1: To examine the parallel between gamma oscillations and the psychometric threshold of perception of Kanizsa square (KS). The latter is gradually altered by a progressive misalignment of lower inducers (pacmen). Results show that the perception of the KS is altered by lateral displacements of the lower inducers as small as 0.1 to 0.2 degrees. In parallel, high frequency components of cortical responses gain in strength with misalignments. 2: Gamma oscillations emerge at or about the psychometric threshold. In addition, our data analysis demonstrates that gamma oscillations appear in short bursts (approx. 50 ms) in the time window between 200 and 500 ms after stimulus onset. Furthermore, controls indicated that these oscillations are of the induced-gamma type. Thus, our experiments suggest that gamma oscillations are associated with image structures and may be induced by local properties of the target.

Visual cells remember earlier applied target: plasticity of orientation selectivity.

BACKGROUND: A canonical proposition states that, in mature brain, neurons responsive to sensory stimuli are tuned to specific properties installed shortly after birth. It is amply demonstrated that that neurons in adult visual cortex of cats are orientation-selective that is they respond with the highest firing rates to preferred oriented stimuli. METHODOLOGY/PRINCIPAL FINDINGS: In anesthetized cats, prepared in a conventional fashion for single cell recordings, the present investigation shows that presenting a stimulus uninterruptedly at a non-preferred orientation for twelve minutes induces changes in orientation preference. Across all conditions orientation tuning curves were investigated using a trial by trial method. Contrary to what has been previously reported with shorter adaptation duration, twelve minutes of adaptation induces mostly attractive shifts, i.e. toward the adapter. After a recovery period allowing neurons to restore their original orientation tuning curves, we carried out a second adaptation which produced three major results: (1) more frequent attractive shifts, (2) an increase of their magnitude, and (3) an additional enhancement of responses at the new or acquired preferred orientation. Additionally, we also show that the direction of shifts depends on the duration of the adaptation: shorter adaptation in most cases produces repulsive shifts, whereas adaptation exceeding nine minutes results in attractive shifts, in the same unit. Consequently, shifts in preferred orientation depend on the duration of adaptation. CONCLUSION/SIGNIFICANCE: The supplementary response improvements indicate that neurons in area 17 keep a memory trace of the previous stimulus properties, thereby upgrading cellular performance. It also highlights the dynamic nature of basic neuronal properties in adult cortex since repeated adaptations modified both the orientation tuning selectivity and the response strength to the preferred orientation. These enhanced neuronal responses suggest that the range of neuronal plasticity available to the visual system is broader than anticipated.