Escaping the nocturnal bottleneck, and the evolution of the dorsal and ventral streams of visual processing in primates

Early mammals were small and nocturnal. Their visual systems had regressed and they had poor vision. After the extinction of the dinosaurs 66 mya, some but not all escaped the ‘nocturnal bottleneck’ by recovering high-acuity vision. By contrast, early primates escaped the bottleneck within the age of dinosaurs by having large forward-facing eyes and acute vision while remaining nocturnal. We propose that these primates differed from other mammals by changing the balance between two sources of visual information to cortex. Thus, cortical processing became less dependent on a relay of information from the superior colliculus (SC) to temporal cortex and more dependent on information distributed from primary visual cortex (V1). In addition, the two major classes of visual information from the retina became highly segregated into magnocellular (M cell) projections from V1 to the primate-specific temporal visual area (MT), and parvocellular-dominated projections to the dorsolateral visual area (DL or V4). The greatly expanded P cell inputs from V1 informed the ventral stream of cortical processing involving temporal and frontal cortex. The M cell pathways from V1 and the SC informed the dorsal stream of cortical processing involving MT, surrounding temporal cortex, and parietal–frontal sensorimotor domains. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Sensory cortical dynamics during optical microstimulation training

Primary sensory cortex is a key locus of plasticity during learning. Exposure to novel stimuli often alters cortical activity, but isolating cortex-specific dynamics is challenging due to extensive pre-cortical processing. Here, we employ optical microstimulation of pyramidal neurons in layer (L) 2/3 of mouse primary vibrissal somatosensory cortex (vS1) to study cortical dynamics as mice learn to discriminate microstimulation intensity. Tracking activity over weeks using two-photon calcium imaging, we observe a rapid sparsification of the photoresponsive population, with the most responsive neurons exhibiting the largest declines in responsiveness. Following sparsification, the photoresponsive population attains a stable rate of neuronal turnover. At the same time, the photoresponsive population increasingly overlaps with populations encoding whisker movement and touch. Finally, we find that mice with larger declines in responsiveness learn the task more slowly than mice with smaller declines. Our results reveal that microstimulation-evoked cortical activity undergoes extensive reorganization during task learning and that the dynamics of this reorganization impact perception.

Functional connectivity and information pathways in the human entorhinal-hippocampal circuitry

Cortical processing streams for item and contextual information come together in the entorhinal-hippocampal circuitry. Various evidence suggest that information-specific pathways organize the cortical — entorhinal interaction and the circuitry's inner communication along the transversal axis. Here, we leveraged ultra-high field functional imaging and advance Maass, Berron et al. (2015) who report two functional routes segregating the entorhinal cortex (EC) and subiculum. Our data show specific scene processing in the functionally connected posterior-medial EC and distal subiculum. The regions of another route, that connects the anterior-lateral EC and a newly identified retrosplenial-based anterior-medial EC subregion with the CA1/subiculum border, process object and scene information similarly. Our results support topographical information flow in human entorhinal-hippocampal subregions with organized convergence of cortical processing streams and a unique route for contextual information. They characterize the functional organization of the circuitry and underpin its central role in memory function and pathological decline.

Looking from the top: enhanced top-down sensorimotor processing in somatic anxiety

BackgroundFunctional neuroimaging research on anxiety has traditionally focused on brain networks associated with the complex psychological aspects of anxiety. In this study, instead, we target the somatic aspects of anxiety. Motivated by the growing recognition that top-down cortical processing plays crucial roles in perception and action, we investigate effective connectivity among hierarchically organized sensorimotor regions and its association with (trait) anxiety.MethodsWe selected 164 participants from the Human Connectome Project based on psychometric measures. We used their resting-state functional MRI data and Dynamic Causal Modeling (DCM) to assess effective connectivity within and between key regions in the exteroceptive, interoceptive, and motor hierarchy. Using hierarchical modeling of between-subject effects in DCM with Parametric Empirical Bayes we first established the architecture of effective connectivity in sensorimotor networks and investigated its association with fear somatic arousal (FSA) and fear affect (FA) scores. To probe the robustness of our results, we implemented a leave-one-out cross validation analysis.ResultsAt the group level, the top-down connections in exteroceptive cortices were inhibitory in nature whereas in interoceptive and motor cortices they were excitatory. With increasing FSA scores, the pattern of top-down effective connectivity was enhanced in all three networks: an observation that corroborates well with anxiety phenomenology. Anxiety associated changes in effective connectivity were of effect size sufficiently large to predict whether somebody has mild or severe somatic anxiety. Interestingly, the enhancement in top-down processing in sensorimotor cortices were associated with FSA but not FA scores, thus establishing the (relative) dissociation between somatic and cognitive dimensions of anxiety.ConclusionsOverall, enhanced top-down effective connectivity in sensorimotor cortices emerges as a promising and quantifiable candidate marker of trait somatic anxiety. These results pave the way for a novel approach into investigating the neural underpinnings of anxiety based on the recognition of anxiety as an embodied phenomenon and the emerging interest in top-down cortical processing.

Individual Stability of Pain- and Touch-Related Neuronal Gamma Oscillations

Background: The processing of brief pain and touch stimuli has been associated with an increase of neuronal oscillations in the gamma range (40-90 Hz). However, some studies report divergent gamma effects across single participants. Methods: In two repeated sessions we recorded gamma responses to pain and touch stimuli using EEG. Individual gamma responses were extracted from EEG channels and from ICA components that contain a strong gamma amplitude. Results: We observed gamma responses in the majority of the participants. If present, gamma synchronisation was always bound to a component that contained a laser-evoked response. We found a broad variety of individual cortical processing: some participants showed a clear gamma effect, others did not exhibit any gamma. For both modalities, the effect was reproducible between sessions. In addition, participants with a strong gamma response showed a similar time-frequency pattern across sessions. Conclusions: Our results indicate that current measures of reproducibility of research results do not reflect the complex reality of the diverse individual processing pattern of applied pain and touch. The present findings raise the question of whether we would find similar quantitatively different processing patterns in other domains in neuroscience: group results would be replicable but the overall effect is driven by a subgroup of the participants.