Attention:The NSF Public Access Repository (PAR) system and access will be unavailable from 5:00 PM ET until 8:00 PM ET on Friday, September 11 due to maintenance. We apologize for the inconvenience.


Title: Context-dependent modulation of natural approach behaviour in mice
Specific features of visual objects innately draw approach responses in animals, and provide natural signals of potential reward. However, visual sampling behaviours and the detection of salient, rewarding stimuli are context and behavioural state-dependent and it remains unclear how visual perception and orienting responses change with specific expectations. To start to address this question, we employed a virtual stimulus orienting paradigm based on prey capture to quantify the conditional expression of visual stimulus-evoked innate approaches in freely moving mice. We found that specific combinations of stimulus features selectively evoked innate approach or freezing responses when stimuli were unexpected. We discovered that prey capture experience, and therefore the expectation of prey in the environment, selectively modified approach frequency, as well as altered those visual features that evoked approach. Thus, we found that mice exhibit robust and selective orienting responses to parameterized visual stimuli that can be robustly and specifically modified via natural experience. This work provides critical insight into how natural appetitive behaviours are driven by both specific features of visual motion and internal states that alter stimulus salience.  more » « less
Award ID(s):
1852578
PAR ID:
10535471
Author(s) / Creator(s):
; ; ; ; ;
Publisher / Repository:
Royal Society
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
287
Issue:
1934
ISSN:
0962-8452
Page Range / eLocation ID:
20201189
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Assessments of the mouse visual system based on spatial-frequency analysis imply that its visual capacity is low, with few neurons responding to spatial frequencies greater than 0.5 cycles per degree. However, visually mediated behaviors, such as prey capture, suggest that the mouse visual system is more precise. We introduce a stimulus class—visual flow patterns—that is more like what the mouse would encounter in the natural world than are sine-wave gratings but is more tractable for analysis than are natural images. We used 128-site silicon microelectrodes to measure the simultaneous responses of single neurons in the primary visual cortex (V1) of alert mice. While holding temporal-frequency content fixed, we explored a class of drifting patterns of black or white dots that have energy only at higher spatial frequencies. These flow stimuli evoke strong visually mediated responses well beyond those predicted by spatial-frequency analysis. Flow responses predominate in higher spatial-frequency ranges (0.15–1.6 cycles per degree), many are orientation or direction selective, and flow responses of many neurons depend strongly on sign of contrast. Many cells exhibit distributed responses across our stimulus ensemble. Together, these results challenge conventional linear approaches to visual processing and expand our understanding of the mouse’s visual capacity to behaviorally relevant ranges. 
    more » « less
  2. Abstract Sensory stimuli evoke spiking neural responses that innately or after learning drive suitable behavioral outputs. How are these spiking activities intrinsically patterned to encode for innate preferences, and could the neural response organization impose constraints on learning? We examined this issue in the locust olfactory system. Using a diverse odor panel, we found that ensemble activities both during (‘ON response’) and after stimulus presentations (‘OFF response’) could be linearly mapped onto overall appetitive preference indices. Although diverse, ON and OFF response patterns generated by innately appetitive odorants (higher palp-opening responses) were still limited to a low-dimensional subspace (a ‘neural manifold’). Similarly, innately non-appetitive odorants evoked responses that were separable yet confined to another neural manifold. Notably, only odorants that evoked neural response excursions in the appetitive manifold could be associated with gustatory reward. In sum, these results provide insights into how encoding for innate preferences can also impact associative learning. 
    more » « less
  3. Recent fMRI studies in human subjects have found affect-specific neural representations of emotional scenes in early visual cortex. The origin of these representations is debated. One group of hypotheses suggests that these representations result from reentrant feedback from anterior emotion-modulating structures (e.g., the amygdala), whereas another group of hypotheses states that sensory cortex, including retinotopic visual cortex, may itself code for the emotional qualities of visual stimuli, without the necessity for feedback processing. We examined this problem by employing a neural encoding model that can generate synthetic fMRI responses to natural images in early visual cortex. The model works by linearly mapping features extracted by convolutional neural networks onto voxel-wise BOLD responses in different visual areas and is trained on the Natural Scenes Dataset. Dividing the images in the International Affective Picture System into three broad categories: pleasant, neutral and unpleasant, we found that in early visual cortex, the neural patterns evoked by the emotional images cannot be decoded from that evoked by the neutral images, in contrast with the findings from recent fMRI studies in human subjects. Because the model-generated responses are free from emotion-modulated reentrant feedback, this finding can be seen as lending support to the reentry hypothesis. Interestingly, when face stimuli from the AffectNet were shown to the model, the neural patterns evoked by emotional faces in early visual cortex can be significantly decoded from that evoked by neutral faces, suggesting that the early visual cortex may contribute differently to the emotional processing of faces versus scenes. 
    more » « less
  4. ABSTRACT Spatially invariant feature detection is a property of many visual systems that rely on visual information provided by two eyes. However, how information across both eyes is integrated for invariant feature detection is not fully understood. Here, we investigated spatial invariance of looming responses in descending neurons (DNs) of Drosophila melanogaster. We found that multiple looming responsive DNs integrate looming information across both eyes, even though their dendrites are restricted to a single visual hemisphere. One DN, the giant fiber (GF), responds invariantly to looming stimuli across tested azimuthal locations. We confirmed visual information propagates to the GF from the contralateral eye, through an unidentified pathway, and demonstrated that the absence of this pathway alters GF responses to looming stimuli presented to the ipsilateral eye. Our data highlight a role for bilateral visual integration in generating consistent, looming-evoked escape responses that are robust across different stimulus locations and parameters. 
    more » « less
  5. Abstract Understanding how genetically-defined cell populations encode visual information remains a fundamental challenge in systems neuroscience. While extensive research has characterized individual cell responses to simple stimuli such as static gratings, the population-level coding principles that govern naturalistic visual processing across cell types remain largely unexplored. We analyzed population responses from 43,018 neurons across 12 genetically-defined cell types in 243 mice from the Allen Brain Observatory, comparing representational geometry between natural scenes and static gratings. We found that inhibitory cell populations (VIP, SST, PV) cluster distinctly in representational space almost independent of anatomical location when responding to natural scenes but not static gratings, suggesting preserved cell-type specific computational functions specific for natural scenes. To assess coding capacity of a population of neurons, we developed Inter-Individual Representational Similarity (IIRS), which measures consistency of neural representations across different individuals in response to an ensemble of stimuli. All inhibitory populations showed significantly higher IIRS for natural scenes compared to static gratings, indicating consistent encoding of naturalistic visual features across individuals comparable to excitatory populations (Cux2, Rorb, Rbp4). Parallel analysis of neural networks trained on natural images (ImageNet) with different random initializations revealed similar patterns: models showed higher cross-initialization similarity for naturalistic stimuli compared to static gratings, suggesting that cross-individual consistency emerges when experimental stimuli engage the features that neural circuits are adapted to extract. These findings establish IIRS as a metric for identifying coding capacity in cell populations and reveal that inhibitory cell populations encode consistent aspects of natural scenes across individuals, indicating these circuits may have evolved specialized tuning for naturalistic visual environments. 
    more » « less