Multi-scale adaptation in brain sensory pathways
Human Cognitive and Systems Neuroscience
Final Report Abstract
Sensory pathways in the brain adapt to the current environment by adjusting neuronal responses to the recent history of stimulation. Adaptation effects occur over a wide range of timescales, but how these timescales interact, and the neuronal mechanisms that support them remain unclear. Moreover, the interaction between adaptation and longer-term plasticity mechanisms such as learning remains largely unknown. The main aim of this project was to investigate the dependence of brain responses on statistical history of stimulation at multiple timescales. We first examined how responses in the superior colliculus are affected by short repeated presentation of the same stimulus. The response of visual neurons is typically suppressed by repeated presentation of an object. Whether this suppression reflects stimulus adaptation or expectation is unclear. We made extracellular recordings from the superficial layers of the superior colliculus in two awake mice while they were presented with small white or black discs which were repeated four times in one spatial location (adaptor). Following presentation of the adaptor, we measured responses to test stimuli of varying contrasts in the same location or adjacent to it. We found that adaptation suppressed responses to test stimuli that had the same polarity and location as the adaptor. Responses to test stimuli in the location adjacent to the adaptor were largely unaffected. This suggests that repetition suppression in the mouse superior colliculus is primarily stimulus adaptation, as an expectation-related signal would be unlikely to show such high spatial specificity. We also found that in some units, responses were suppressed only for test stimuli of matched polarity, particularly following adaptation to the black discs. In other units, responses to both polarities were strongly suppressed, particularly following adaptation to the white discs. The partial polarity-specificity suggests that this adaptation occurs in parallel input pathways. In a second set of experiments, we aimed to examine how the adaptation state induced by one environment interacts with that induced by subsequent environments. We recorded from the primary visual cortex of six awake mice in response to a vertical bar that randomly varied in horizontal location. The ensemble of bar locations was either uniform, or biased to one location. After initial exposure to a uniform ensemble, we presented a biased ensemble for 5-minutes. Biasing the stimulus ensemble decreased the gain of neurons with receptive fields near the adaptor, and repulsed receptive fields away from the adaptor. The reduction in gain was rapid while the repulsion of the receptive fields was slower, accumulating over at least 3 minutes. This suggests dissociation of adaptation-induced changes in gain and receptive field organisation. To assess the persistence of adaptation-induced changes, following the initial adaptation period we returned to the uniform stimulus ensemble for 1 minute, then repeated the biased ensemble for another 5-minutes. The magnitude and timecourse of gain changes in this second adaptation period was similar to that in the first. By contrast, we saw stronger, and quicker repulsion of receptive field profiles in the second biased ensemble. This suggests that traces of the previously adapted state were retained in the neuronal population. In another experiment, 5-minutes exposure to one location bias was followed by 1-minute exposure to a new location bias. The second bias decreased the gain and repulsed the receptive fields of neurons around the newly adapted location. Neurons near the location of the original bias showed small increase in gain, but no change in receptive field profile. A mixture of both adaptation states was maintained during subsequent exposure to uniform ensembles. Our observations suggest that changes in environmental statistics lead to rapid recalibration in the sensitivity of neuronal responses and slower, potentially long-lasting changes in receptive field organisation, suggesting at least two distinct mechanisms of adaptation that operate over different timescales. Finally, we aimed to examine how short-term adaptation relates to learning. Both adaptation and learning have been intensively studied in isolation. However, the interaction between these distinct forms of plasticity remains largely unknown. We recorded from layer 4 in V1 of two awake mice using chronically implanted microelectrodes while they were presented with a stimulus of a single orientation (familiar) over the course of 9 days. We compared responses to the familiar stimulus with a grating of a different orientation (novel stimulus) presented in the first and last day. To assess the effects of adaptation within each session we presented test stimuli of 6 orientations before and after presentation of the familiar or the novel stimulus. We found that 9 days familiarization to one orientation leads to orientation-specific enhancement in the LFP response of mouse V1 consistent with previous reports. No orientation specific adaptation was observed in the LFP signal over the course of days. However, initial results show that training to one orientation induced less adaptive changes in the spiking activity of neurons over the course of days suggesting that that there is a neuronal relationship between adaptation and learning. This project has examined how neuronal responses in the mouse visual system depend on stimulus history at multiple timescales. Our observations show that the brain keeps a “memory” trace of previous adapted states. Future research of the relationship between adaptation and learning are warranted to improve our understand of plasticity mechanisms in the brain.
Publications
- (2017) Interaction of adaptation states in the mouse primary visual cortex. AVA Xmas meeting, Queen Mary University of London, London, UK, PERCEPTION 47 (5): 567-567
A Papanikolaou, De Franceschi G, & Solomon SG
- (2017) Spatial and luminance specificity of repetition suppression in superior colliculus of awake mice. AVA Xmas meeting, Queen Mary University of London, London, UK, Perception 47 (5): 576-577
SG Solomon, De Franceschi G, & Papanikolaou A
- (2018) Timescales of adaptation in the primary visual cortex of awake mice. Program No. 142.17. 2018 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2018
A Papanikolaou, De Franceschi G, & Solomon SG
- (2019) Organization of area hV5/MT+ in subjects with homonymous visual field defects, NeuroImage 190: 254-268
A Papanikolaou, Keliris GA, Papageorgiou TD, Schiefer U, Logothetis NK, Smirnakis SM
(See online at https://doi.org/10.1016/j.neuroimage.2018.03.062)
