Effects of arousal and movement on secondary somatosensory and visual thalamus

Neocortical sensory areas have associated primary and secondary thalamic nuclei. While primary nuclei transmit sensory information to cortex, secondary nuclei remain poorly understood. We recorded juxtasomally from secondary somatosensory (POm) and visual (LP) nuclei of awake mice while tracking whisking and pupil size. POm activity correlated with whisking, but not precise whisker kinematics. This coarse movement modulation persisted after facial paralysis and thus was not due to sensory reafference. This phenomenon also continued during optogenetic silencing of somatosensory and motor cortex and after lesion of superior colliculus, ruling out a motor efference copy mechanism. Whisking and pupil dilation were strongly correlated, possibly reflecting arousal. Indeed LP, which is not part of the whisker system, tracked whisking equally well, further indicating that POm activity does not encode whisker movement per se. The semblance of movement-related activity is likely instead a global effect of arousal on both nuclei. We conclude that secondary thalamus monitors behavioral state, rather than movement, and may exist to alter cortical activity accordingly.

Short-term plasticity in the visual thalamus

While there is evidence that the visual cortex retains a potential for plasticity in adulthood, less is known about the subcortical stages of visual processing. Here we asked whether short-term ocular dominance plasticity affects the visual thalamus. We addressed this question in normally sighted adult humans, using ultra-high field (7T) magnetic resonance imaging combined with the paradigm of short-term monocular deprivation. With this approach, we previously demonstrated transient shifts of perceptual eye dominance and ocular dominance in visual cortex (Binda et al., 2018). Here we report evidence for short-term plasticity in the ventral division of the pulvinar (vPulv), where the deprived eye representation was enhanced over the non-deprived eye. This pulvinar plasticity effect was similar as previously seen in visual cortex and it was correlated with the ocular dominance shift measured behaviorally. In contrast, there was no short-term plasticity effect in Lateral Geniculate Nucleus (LGN), where results were reliably different from vPulv, despite their spatial proximity. We conclude that the visual thalamus retains potential for short-term plasticity in adulthood; the plasticity effect differs across thalamic subregions, possibly reflecting differences in their cortical connectivity.

Fast unconscious processing of emotional stimuli in early stages of the visual cortex

Several cortical and subcortical brain areas have been reported to be sensitive to the emotional content of subliminal stimuli. However, the timing of these activations remains unclear. Our scope was to detect the earliest cortical traces of visual unconscious processing by recording event-related potentials (ERPs) from 43 participants. Subliminal spiders (emotional) and wheels (neutral), sharing similar low-level visual parameters, were presented at two different locations (fixation and periphery). The differential (peak to peak) amplitude from CP1 (77 milliseconds from stimulus onset) to C2 (100 milliseconds), two early visual ERP components originated in V1/V2 according to source localization analyses, was analyzed via Bayesian and traditional analyses. Spiders elicited greater CP1-C2 amplitudes than wheels when presented at fixation. This fast effect of subliminal stimulation -not reported previously to the best of our knowledge- has implications in several debates: i) the amygdala cannot be mediating these effects, ii) latency of other evaluative structures recently proposed, such as the visual thalamus, is compatible with these results, iii) the absence of peripheral stimuli effects points to a relevant role of the parvocellular visual system in unconscious processing.

The Missing Link in Early Emotional Processing

Initial evaluation structures (IESs) currently proposed as the earliest detectors of affective stimuli (e.g., amygdala, orbitofrontal cortex, or insula) are high-order structures (a) whose response latency cannot account for the first visual cortex emotion-related response (~80 ms), and (b) lack the necessary infrastructure to locally analyze the visual features that define emotional stimuli. Several thalamic structures accomplish both criteria. The lateral geniculate nucleus (LGN), a first-order thalamic nucleus that actively processes visual information, with the complement of the thalamic reticular nucleus (TRN) are proposed as core IESs. This LGN–TRN tandem could be supported by the pulvinar, a second-order thalamic structure, and by other extrathalamic nuclei. The visual thalamus, scarcely explored in affective neurosciences, seems crucial in early emotional evaluation.

The Missing Link in Early Emotional Processing

Current proposals on the temporal sequence in the processing of emotional visual stimuli are partially incompatible with growing empirical data. In the majority of them, the initial evaluation structures (IES) postulated to be in charge of the earliest detection of emotional stimuli (i.e., salient for the individual), are high order structures (i.e., those receiving visual inputs after several synapses). Thus, their latency of response cannot account for the first visual cortex response to emotional stimuli (peaking 80 ms in humans). Additionally, these proposed structures lack the necessary infrastructure to locally analyze the visual features of the stimulus (shape, color, motion, etc.) that define a stimulus as emotional. In particular, the amygdala is defended as the cornerstone IES also in humans, and cortical areas such as the ventral prefrontal cortex or the insula have been proposed as well to intervene in this initial evaluation process. The present review describes several first-order brain structures (i.e., receiving visual inputs after one synapsis), and second order structures (two synapses) that may complement the former, that accomplish with both prerequisites: presenting response latencies compatible with the observed activity at the visual cortex and possessing the necessary architecture to rudimentarily analyze in situ relevant features of the visual stimulation. The visual thalamus, and particularly the lateral geniculate nucleus (LGN), a first-order thalamic nucleus that actively processes visual information, is a good candidate to be the core IES, with the complementary action of the thalamic reticular nucleus (TRN). This LGN-TRN tandem could be supported, also in an ascending, initial evaluation phase, by the pulvinar, a second order thalamic structure, and first-order extra-thalamic nuclei (superior colliculus and certain nuclei of pretectum and the accessory optic system). In sum, the visual thalamus, scarcely studied in relation to emotional processing, is a serious candidate to be the missing link in early emotional evaluation and, in any case, is worth exploring in future research.