Sensory computations in the cuneate nucleus of macaques

Tactile nerve fibers fall into a few classes that can be readily distinguished based on their spatiotemporal response properties. Because nerve fibers reflect local skin deformations, they individually carry ambiguous signals about object features. In contrast, cortical neurons exhibit heterogeneous response properties that reflect computations applied to convergent input from multiple classes of afferents, which confer to them a selectivity for behaviorally relevant features of objects. The conventional view is that these complex response properties arise within the cortex itself, implying that sensory signals are not processed to any significant extent in the two intervening structures—the cuneate nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in the CN to a battery of stimuli that have been extensively used to characterize tactile coding in both the periphery and cortex, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their cortical counterparts than they are to their inputs: CN neurons receive input from multiple classes of nerve fibers, they have spatially complex receptive fields, and they exhibit selectivity for object features. Contrary to consensus, then, the CN plays a key role in processing tactile information.

Sensory computations in the cuneate nucleus of macaques

In primates, the responses of individual neurons in primary somatosensory cortex (S1) reflect convergent input from multiple classes of nerve fibers and are selective for behaviorally relevant stimulus features. The conventional view is that these response properties reflect computations that are effected in cortex, implying that sensory signals are not meaningfully processed in the two intervening structures - the Cuneate Nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in CN to a battery of stimuli that have been extensively used to characterize tactile coding, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their S1 counterparts than they are to their inputs: CN neurons receive input from multiple sub-modalities, have spatially complex receptive fields, and exhibit selectivity for geometric features. Thus, CN plays a key role in the processing of tactile information.

Comparing the influence of stimulus size and contrast on the perception of moving gratings and random dot patterns—A registered report protocol

Modern accounts of visual motion processing in the primate brain emphasize a hierarchy of different regions within the dorsal visual pathway, especially primary visual cortex (V1) and the middle temporal area (MT). However, recent studies have called the idea of a processing pipeline with fixed contributions to motion perception from each area into doubt. Instead, the role that each area plays appears to depend on properties of the stimulus as well as perceptual history. We propose to test this hypothesis in human subjects by comparing motion perception of two commonly used stimulus types: drifting sinusoidal gratings (DSGs) and random dot patterns (RDPs). To avoid potential biases in our approach we are pre-registering our study. We will compare the effects of size and contrast levels on the perception of the direction of motion for DSGs and RDPs. In addition, based on intriguing results in a pilot study, we will also explore the effects of a post-stimulus mask. Our approach will offer valuable insights into how motion is processed by the visual system and guide further behavioral and neurophysiological research.

Visual motion integration of bidirectional transparent motion in mouse opto-locomotor reflexes

Visual motion perception depends on readout of direction selective sensors. We investigated in mice whether the response to bidirectional transparent motion, activating oppositely tuned sensors, reflects integration (averaging) or winner-take-all (mutual inhibition) mechanisms. We measured whole body opto-locomotor reflexes (OLRs) to bidirectional oppositely moving random dot patterns (leftward and rightward) and compared the response to predictions based on responses to unidirectional motion (leftward or rightward). In addition, responses were compared to stimulation with stationary patterns. When comparing OLRs to bidirectional and unidirectional conditions, we found that the OLR to bidirectional motion best fits an averaging model. These results reflect integration mechanisms in neural responses to contradicting sensory evidence as has been documented for other sensory and motor domains.

Stereomotion Processing in the Nonhuman Primate Brain

The cortical areas that process disparity-defined motion-in-depth (i.e., cyclopean stereomotion [CSM]) were characterized with functional magnetic resonance imaging (fMRI) in two awake, behaving macaques. The experimental protocol was similar to previous human neuroimaging studies. We contrasted the responses to dynamic random-dot patterns that continuously changed their binocular disparity over time with those to a control condition that shared the same properties, except that the temporal frames were shuffled. A whole-brain voxel-wise analysis revealed that in all four cortical hemispheres, three areas showed consistent sensitivity to CSM. Two of them were localized respectively in the lower bank of the superior temporal sulcus (CSMSTS) and on the neighboring infero-temporal gyrus (CSMITG). The third area was situated in the posterior parietal cortex (CSMPPC). Additional regions of interest-based analyses within retinotopic areas defined in both animals indicated weaker but significant responses to CSM within the MT cluster (most notably in areas MSTv and FST). Altogether, our results are in agreement with previous findings in both human and macaque and suggest that the cortical areas that process CSM are relatively well preserved between the two primate species.

Monkey EEG links neuronal color and motion information across species and scales

It remains challenging to relate EEG and MEG to underlying circuit processes and comparable experiments on both spatial scales are rare. To close this gap between invasive and non-invasive electrophysiology we developed and recorded human-comparable EEG in macaque monkeys during visual stimulation with colored dynamic random dot patterns. Furthermore, we performed simultaneous microelectrode recordings from 6 areas of macaque cortex and human MEG. Motion direction and color information were accessible in all signals. Tuning of the non-invasive signals was similar to V4 and IT, but not to dorsal and frontal areas. Thus, MEG and EEG were dominated by early visual and ventral stream sources. Source level analysis revealed corresponding information and latency gradients across cortex. We show how information-based methods and monkey EEG can identify analogous properties of visual processing in signals spanning spatial scales from single units to MEG – a valuable framework for relating human and animal studies.

Stereomotion processing in the non-human primate brain

The cortical areas that process disparity-defined motion-in-depth (i.e. cyclopean stereomotion) were characterised with functional magnetic resonance imaging in two awake, behaving macaques. The experimental protocol was similar to previous human neuroimaging studies. We contrasted the responses to dynamic random-dot patterns that continuously changed their binocular disparity over time with those to a control condition that shared the same properties, except that the temporal frames were shuffled. A whole-brain voxel-wise analysis revealed that in all four cortical hemispheres, three areas showed consistent sensitivity to cyclopean stereomotion. Two of them were localised respectively in the lower bank of the superior temporal sulcus (CSMSTS) and on the neighbouring infero-temporal gyrus (CSMITG). The third area was situated in the posterior parietal cortex (CSMPPC). Additional ROIs-based analyses within retinotopic areas defined in both animals indicated weaker but significant responses to cyclopean stereomotion within the MT cluster (most notably in areas MSTv and FST). Altogether, our results are in agreement with previous findings in both human and macaque and suggest that the cortical networks that process cyclopean stereomotion is relatively well preserved between the two primate species.

Visual objects interact differently during encoding and memory maintenance

The storage mechanisms of working memory are the matter of an ongoing debate. The sensory recruitment hypothesis states that memory maintenance and perceptual encoding rely on the same neural substrate. This suggests that the same cortical mechanisms that shape object perception also apply to maintained memory content. We tested this prediction using the Direction Illusion, i.e., the mutual repulsion of two concurrently visible motion directions. Participants memorized the directions of two random dot patterns for later recall. In Experiments 1 and 2, we varied the temporal separation of spatially distinct stimuli to manipulate perceptual concurrency, while keeping concurrency within working memory constant. We observed mutual motion repulsion only under simultaneous stimulus presentation, but proactive repulsion and retroactive attraction under immediate stimulus succession. At inter-stimulus intervals of 0.5 and 2 s, however, proactive repulsion vanished, while the retroactive attraction remained. In Experiment 3, we presented both stimuli at the same spatial position and observed a reappearance of the repulsion effect. Our results indicate that the repulsive mechanisms that shape object perception across space fade during the transition from a perceptual representation to a consolidated memory content. This suggests differences in the underlying structure of perceptual and mnemonic representations. The persistence of local interactions, however, indicates different mechanisms of spatially global and local feature interactions.

Monkey EEG links neuronal color and motion information across species and scales

It remains challenging to relate EEG and MEG to underlying circuit processes and comparable experiments on both spatial scales are rare. To close this gap between invasive and non-invasive electrophysiology we developed and recorded human-comparable EEG in macaque monkeys during visual stimulation with colored dynamic random dot patterns. Furthermore, we performed simultaneous microelectrode recordings from 6 areas of macaque cortex and human MEG. Motion direction and color information were accessible in all signal types. Tuning of the non-invasive signals was similar to V4 and IT, but not to dorsal and frontal areas. Thus, MEG and EEG were dominated by early visual and ventral stream sources. Source level analysis revealed corresponding information and latency gradients across the cortex. We show how information-based methods and monkey EEG can identify analogous properties of visual processing in signals spanning spatial scales from single units to MEG – a valuable framework for relating human and animal studies.