Jose-Manuel Alonso

Temporal precision in the neural code and the timescales of natural vision.

The timing of action potentials relative to sensory stimuli can be precise down to milliseconds in the visual system, even though the relevant timescales of natural vision are much slower. The existence of such precision contributes to a fundamental debate over the basis of the neural code and, specifically, what timescales are important for neural computation. Using recordings in the lateral geniculate nucleus, here we demonstrate that the relevant timescale of neuronal spike trains depends on the frequency content of the visual stimulus, and that ‘relative’, not absolute, precision is maintained both during spatially uniform white-noise visual stimuli and naturalistic movies. Using information-theoretic techniques, we demonstrate a clear role of relative precision, and show that the experimentally observed temporal structure in the neuronal response is necessary to represent accurately the more slowly changing visual world. By establishing a functional role of precision, we link visual neuron function on slow timescales to temporal structure in the response at faster timescales, and uncover a straightforward purpose of fine-timescale features of neuronal spike trains.

Task difficulty modulates the activity of specific neuronal populations in primary visual cortex

Spatial attention enhances our ability to detect stimuli at restricted regions of the visual field. This enhancement is thought to depend on the difficulty of the task being performed, but the underlying neuronal mechanisms for this dependency remain largely unknown. We found that task difficulty modulates neuronal firing rate at the earliest stages of cortical visual processing (area V1) in monkey (Macaca mulatta). These modulations were spatially specific: increasing task difficulty enhanced V1 neuronal firing rate at the focus of attention and suppressed it in regions surrounding the focus. Moreover, we found that response enhancement and suppression are mediated by distinct populations of neurons that differ in direction selectivity, spike width, interspike-interval distribution and contrast sensitivity. Our results provide strong support for center-surround models of spatial attention and suggest that task difficulty modulates the activity of specific populations of neurons in the primary visual cortex.

On and off domains of geniculate afferents in cat primary visual cortex

On- and off-center geniculate afferents form two major channels of visual processing that are thought to converge in the primary visual cortex. However, humans with severely reduced on responses can have normal visual acuity when tested in a white background, which indicates that off channels can function relatively independently from on channels under certain conditions. Consistent with this functional independence of channels, we demonstrate here that on- and off-center geniculate afferents segregate in different domains of the cat primary visual cortex and that off responses dominate the cortical representation of the area centralis. On average, 70% of the geniculate afferents converging at the same cortical domain had receptive fields of the same contrast polarity. Moreover, off-center afferents dominated the representation of the area centralis in the cortex, but not in the thalamus, indicating that on- and off-center afferents are balanced in number, but not in the amount of cortical territory that they cover.

Adaptation to stimulus contrast and correlations during natural visual stimulation

In this study, we characterize the adaptation of neurons in the cat lateral geniculate nucleus to changes in stimulus contrast and correlations. By comparing responses to high- and low-contrast natural scene movie and white noise stimuli, we show that an increase in contrast or correlations results in receptive fields with faster temporal dynamics and stronger antagonistic surrounds, as well as decreases in gain and selectivity. We also observe contrast- and correlation-induced changes in the reliability and sparseness of neural responses. We find that reliability is determined primarily by processing in the receptive field (the effective contrast of the stimulus), while sparseness is determined by the interactions between several functional properties. These results reveal a number of adaptive phenomena and suggest that adaptation to stimulus contrast and correlations may play an important role in visual coding in a dynamic natural environment.

The linearity and selectivity of neuronal responses in awake visual cortex

Neurons in primary visual cortex (V1) are frequently classified based on their response linearity: the extent to 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 the 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.

Salience of unique hues and implications for color theory

The unique hues--blue, green, yellow, red--form the fundamental dimensions of opponent-color theories, are considered universal across languages, and provide useful mental representations for structuring color percepts. However, there is no neural evidence for them from neurophysiology or low-level psychophysics. Tapping a higher prelinguistic perceptual level, we tested whether unique hues are particularly salient in search tasks. We found no advantage for unique hues over their nonunique complementary colors. However, yellowish targets were detected faster, more accurately, and with fewer saccades than their complementary bluish targets (including unique blue), while reddish-greenish pairs were not significantly different in salience. Similarly, local field potentials in primate V1 exhibited larger amplitudes and shorter latencies for yellowish versus bluish stimuli, whereas this effect was weaker for reddish versus greenish stimuli. Consequently, color salience is affected more by early neural response asymmetries than by any possible mental or neural representation of unique hues.

Modulation of Temporal Precision in Thalamic Population Responses to Natural Visual Stimuli

Natural visual stimuli have highly structured spatial and temporal properties which influence the way visual information is encoded in the visual pathway. In response to natural scene stimuli, neurons in the lateral geniculate nucleus (LGN) are temporally precise – on a time scale of 10–25 ms – both within single cells and across cells within a population. This time scale, established by non stimulus-driven elements of neuronal firing, is significantly shorter than that of natural scenes, yet is critical for the neural representation of the spatial and temporal structure of the scene. Here, a generalized linear model (GLM) that combines stimulus-driven elements with spike-history dependence associated with intrinsic cellular dynamics is shown to predict the fine timing precision of LGN responses to natural scene stimuli, the corresponding correlation structure across nearby neurons in the population, and the continuous modulation of spike timing precision and latency across neurons. A single model captured the experimentally observed neural response, across different levels of contrasts and different classes of visual stimuli, through interactions between the stimulus correlation structure and the nonlinearity in spike generation and spike history dependence. Given the sensitivity of the thalamocortical synapse to closely timed spikes and the importance of fine timing precision for the faithful representation of natural scenes, the modulation of thalamic population timing over these time scales is likely important for cortical representations of the dynamic natural visual environment.

Push-Pull Receptive Field Organization and Synaptic Depression: Mechanisms for Reliably Encoding Naturalistic Stimuli in V1

Neurons in the primary visual cortex are known for responding vigorously but with high variability to classical stimuli such as drifting bars or gratings. By contrast, natural scenes are encoded more efficiently by sparse and temporal precise spiking responses. We used a conductance-based model of the visual system in higher mammals to investigate how two specific features of the thalamo-cortical pathway, namely push-pull receptive field organization and fast synaptic depression, can contribute to this contextual reshaping of V1 responses. By comparing cortical dynamics evoked respectively by natural vs. artificial stimuli in a comprehensive parametric space analysis, we demonstrate that the reliability and sparseness of the spiking responses during natural vision is not a mere consequence of the increased bandwidth in the sensory input spectrum. Rather, it results from the combined impacts of fast synaptic depression and push-pull inhibition, the later acting for natural scenes as a form of “effective” feed-forward inhibition as demonstrated in other sensory systems. Thus, the combination of feedforward-like inhibition with fast thalamo-cortical synaptic depression by simple cells receiving a direct structured input from thalamus composes a generic computational mechanism for generating a sparse and reliable encoding of natural sensory events.

My recollections of Hubel and Wiesel and a brief review of functional circuitry in the visual pathway

The first paper of Hubel and Wiesel in The Journal of Physiology in 1959 marked the beginning of an exciting chapter in the history of visual neuroscience. Through a collaboration that lasted 25 years, Hubel and Wiesel described the main response properties of visual cortical neurons, the functional architecture of visual cortex and the role of visual experience in shaping cortical architecture. The work of Hubel and Wiesel transformed the field not only through scientific discovery but also by touching the life and scientific careers of many students. Here, I describe my personal experience as a postdoctoral student with Torsten Wiesel and how this experience influenced my own work.

Spikes are making waves in the visual cortex

Cortical and thalamic contribution to V1 neuron response properties is thought to be fixed. New work overturns this assumption, showing that the spread of corticocortical activation can be strongly modulated by stimulus strength.