Perceptual experiences may arise from neuronal activity patterns in mammalian neocortex. We probed mouse neocortex during visual discrimination using a red-shifted channelrhodopsin (ChRmine, discovered through structure-guided genome mining) alongside multiplexed multiphoton-holography (MultiSLM), achieving control of individually specified neurons spanning large cortical volumes with millisecond precision. Stimulating a critical number of stimulus-orientation-selective neurons drove widespread recruitment of functionally related neurons, a process enhanced by (but not requiring) orientation-discrimination task learning. Optogenetic targeting of orientation-selective ensembles elicited correct behavioral discrimination. Cortical layer–specific dynamics were apparent, as emergent neuronal activity asymmetrically propagated from layer 2/3 to layer 5, and smaller layer 5 ensembles were as effective as larger layer 2/3 ensembles in eliciting orientation discrimination behavior. Population dynamics emerging after optogenetic stimulation both correctly predicted behavior and resembled natural internal representations of visual stimuli at cellular resolution over volumes of cortex.
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Long time no see: enduring behavioral and neuronal changes in perceptual learning of motion trajectories 3 years after training.
Here, we report on the long-term stability of changes in behavior and brain activity following perceptual learning of conjunctions of simple motion features. Participants were trained for 3 weeks on a visual search task involving the detection of a dot moving in a “v”-shaped target trajectory among inverted “v”-shaped distractor trajectories. The first and last training sessions were carried out during functional magnetic resonance imaging (fMRI). Learning stability was again examined behaviorally and using fMRI 3 years after the end of training. Results show that acquired behavioral improvements were remarkably stable over time and that these changes were specific to trained target and distractor trajectories. A similar pattern was observed on the neuronal level, when the representation of target and distractor stimuli was examined in early retinotopic visual cortex (V1–V3): training enhanced activity for the target relative to the surrounding distractors in the search array and this enhancement persisted after 3 years. However, exchanging target and distractor trajectories abolished both neuronal and behavioral effects, suggesting that training-induced changes in stimulus representation are specific to trained stimulus identities.
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- Award ID(s):
- 1632738
- NSF-PAR ID:
- 10025808
- Date Published:
- Journal Name:
- Cerebral cortex
- ISSN:
- 1047-3211
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Investigations into how individual neurons encode behavioral variables of interest have revealed specific representations in single neurons, such as place and object cells, as well as a wide range of cells with conjunctive encodings or mixed selectivity. However, as most experiments examine neural activity within individual tasks, it is currently unclear if and how neural representations change across different task contexts. Within this discussion, the medial temporal lobe is particularly salient, as it is known to be important for multiple behaviors including spatial navigation and memory, however the relationship between these functions is currently unclear. Here, to investigate how representations in single neurons vary across different task contexts in the medial temporal lobe, we collected and analyzed single‐neuron activity from human participants as they completed a paired‐task session consisting of a passive‐viewing visual working memory and a spatial navigation and memory task. Five patients contributed 22 paired‐task sessions, which were spike sorted together to allow for the same putative single neurons to be compared between the different tasks. Within each task, we replicated concept‐related activations in the working memory task, as well as target‐location and serial‐position responsive cells in the navigation task. When comparing neuronal activity between tasks, we first established that a significant number of neurons maintained the same kind of representation, responding to stimuli presentations across tasks. Further, we found cells that changed the nature of their representation across tasks, including a significant number of cells that were stimulus responsive in the working memory task that responded to serial position in the spatial task. Overall, our results support a flexible encoding of multiple, distinct aspects of different tasks by single neurons in the human medial temporal lobe, whereby some individual neurons change the nature of their feature coding between task contexts.
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The current study examined the neural correlates of spatial rotation in eight engineering undergraduates. Mastering engineering graphics requires students to mentally visualize in 3D and mentally rotate parts when developing 2D drawings. Students’ spatial rotation skills play a significant role in learning and mastering engineering graphics. Traditionally, the assessment of students’ spatial skills involves no measurements of neural activity during student performance of spatial rotation tasks. We used electroencephalography (EEG) to record neural activity while students performed the Revised Purdue Spatial Visualization Test: Visualization of Rotations (Revised PSVT:R). The two main objectives were to 1) determine whether high versus low performers on the Revised PSVT:R show differences in EEG oscillations and 2) identify EEG oscillatory frequency bands sensitive to item difficulty on the Revised PSVT:R. Overall performance on the Revised PSVT:R determined whether participants were considered high or low performers: students scoring 90% or higher were considered high performers (5 students), whereas students scoring under 90% were considered low performers (3 students). Time-frequency analysis of the EEG data quantified power in several oscillatory frequency bands (alpha, beta, theta, gamma, delta) for comparison between low and high performers, as well as between difficulty levels of the spatial rotation problems. Although we did not find any significant effects of performance type (high, low) on EEG power, we observed a trend in reduced absolute delta and gamma power for hard problems relative to easier problems. Decreases in delta power have been reported elsewhere for difficult relative to easy arithmetic calculations, and attributed to greater external attention (e.g., attention to the stimuli/numbers), and consequently, reduced internal attention (e.g., mentally performing the calculation). In the current task, a total of three spatial objects are presented. An example rotation stimulus is presented, showing a spatial object before and after rotation. A target stimulus, or spatial object before rotation is then displayed. Students must choose one of five stimuli (multiple choice options) that indicates the correct representation of the object after rotation. Reduced delta power in the current task implies that students showed greater attention to the example and target stimuli for the hard problem, relative to the moderate and easy problems. Therefore, preliminary findings suggest that students are less efficient at encoding the target stimuli (external attention) prior to mental rotation (internal attention) when task difficulty increases. Our findings indicate that delta power may be used to identify spatial rotation items that are especially challenging for students. We may then determine the efficacy of spatial rotation interventions among engineering education students, using delta power as an index for increases in internal attention (e.g., increased delta power). Further, in future work, we will also use eye-tracking to assess whether our intervention decreases eye fixation (e.g., time spent viewing) toward the target stimulus on the Revised PSVT:R. By simultaneously using EEG and eye-tracking, we may identify changes in internal attention and encoding of the target stimuli that are predictive of improvements in spatial rotation skills among engineering education students.more » « less
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Abstract The development of the ability to anticipate—as manifested by preparatory actions and neural activation related to the expectation of an upcoming stimulus—may play a key role in the ontogeny of cognitive skills more broadly. This preregistered study examined anticipatory brain potentials and behavioral responses (reaction time; RT) to anticipated target stimuli in relation to individual differences in the ability to use goals to direct action (as indexed by measures of executive function; EF). A cross‐sectional investigation was conducted in 40 adults (aged 18–25 years) and 40 children (aged 6–8 years) to examine the association of changes in the amplitude of modality‐specific alpha‐range rhythms in the electroencephalogram (EEG) during anticipation of lateralized visual, tactile, or auditory stimuli with inter‐ and intraindividual variation in RT and EF. Children and adults exhibited contralateral anticipatory reductions in the mu rhythm and the visual alpha rhythm for tactile and visual anticipation, respectively, indicating modality and spatially specific attention allocation. Variability in within‐subject anticipatory alpha lateralization (the difference between contralateral and ipsilateral alpha power) was related to single‐trial RT. This relation was more prominent in adults than in children, and was not apparent for auditory stimuli. Multilevel models indicated that interindividual differences in anticipatory mu rhythm lateralization contributed to the significant association with variability in EF, but this was not the case for visual or auditory alpha rhythms. Exploratory microstate analyses were undertaken to cluster global field power (GFP) into a distribution‐free temporal analysis examining developmental differences across samples and in relation to RT and EF. Anticipation is suggested as a developmental bridge construct connecting neuroscience, behavior, and cognition, with anticipatory EEG oscillations being discussed as quantifiable and potentially malleable indicators of stimulus prediction.
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The macaque middle temporal (MT) area is well known for its visual motion selectivity and relevance to motion perception, but the possibility of it also reflecting higher-level cognitive functions has largely been ignored. We tested for effects of task performance distinct from sensory encoding by manipulating subjects' temporal evidence-weighting strategy during a direction discrimination task while performing electrophysiological recordings from groups of MT neurons in rhesus macaques (one male, one female). This revealed multiple components of MT responses that were, surprisingly, not interpretable as behaviorally relevant modulations of motion encoding, or as bottom-up consequences of the readout of motion direction from MT. The time-varying motion-driven responses of MT were strongly affected by our strategic manipulation—but with time courses opposite the subjects' temporal weighting strategies. Furthermore, large choice-correlated signals were represented in population activity distinct from its motion responses, with multiple phases that lagged psychophysical readout and even continued after the stimulus (but which preceded motor responses). In summary, a novel experimental manipulation of strategy allowed us to control the time course of readout to challenge the correlation between sensory responses and choices, and population-level analyses of simultaneously recorded ensembles allowed us to identify strong signals that were so distinct from direction encoding that conventional, single-neuron-centric analyses could not have revealed or properly characterized them. Together, these approaches revealed multiple cognitive contributions to MT responses that are task related but not functionally relevant to encoding or decoding of motion for psychophysical direction discrimination, providing a new perspective on the assumed status of MT as a simple sensory area.
SIGNIFICANCE STATEMENT This study extends understanding of the middle temporal (MT) area beyond its representation of visual motion. Combining multineuron recordings, population-level analyses, and controlled manipulation of task strategy, we exposed signals that depended on changes in temporal weighting strategy, but did not manifest as feedforward effects on behavior. This was demonstrated by (1) an inverse relationship between temporal dynamics of behavioral readout and sensory encoding, (2) a choice-correlated signal that always lagged the stimulus time points most correlated with decisions, and (3) a distinct choice-correlated signal after the stimulus. These findings invite re-evaluation of MT for functions outside of its established sensory role and highlight the power of experimenter-controlled changes in temporal strategy, coupled with recording and analysis approaches that transcend the single-neuron perspective.
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Accepted Manuscript1.0
- Journal Article:
- The DOI is not currently available.
