Sensory prediction errors increase coding efficiency in mouse visual cortex through gain amplification

Abstract The efficiency of sensory coding is affected both by past events (adaptation) and by expectation of future events (prediction). Here we employed a novel visual stimulus paradigm to determine whether expectation influences orientation selectivity in the primary visual cortex. We used two-photon calcium imaging (GCaMP6f) in awake mice viewing visual stimuli with different levels of predictability. The stimuli consisted of sequences of grating stimuli that randomly shifted in orientation or systematically rotated with occasionally unexpected rotations. At the single neuron and population level, there was significantly enhanced orientation-selective response to unexpected visual stimuli through a boost in gain, which was prominent in awake mice but also present to a lesser extent under anesthesia. We implemented a computational model to demonstrate how neuronal responses were best characterized when adaptation and expectation parameters were combined. Our results demonstrated that adaptation and prediction have unique signatures on activity of V1 neurons.

Download Full-text

Sensory prediction errors increase coding efficiency in mouse visual cortex through gain amplification

10.1101/2021.10.26.466004 ◽

2021 ◽

Author(s):

Matthew F Tang ◽

Ehsan Kheradpezhouh ◽

Conrad CY Lee ◽

J Edwin Dickinson ◽

Jason B Mattingley ◽

...

Keyword(s):

Visual Cortex ◽

Visual Stimuli ◽

Population Level ◽

Prediction Errors ◽

V1 Neurons ◽

Coding Efficiency ◽

Two Photon ◽

Future Events ◽

Mouse Visual Cortex ◽

Sensory Prediction

The efficiency of sensory coding is affected both by past events (adaptation) and by expectation of future events (prediction). Here we employed a novel visual stimulus paradigm to determine whether expectation influences orientation selectivity in the primary visual cortex. We used two-photon calcium imaging (GCaMP6f) in awake mice viewing visual stimuli with different levels of predictability. The stimuli consisted of sequences of grating stimuli that randomly shifted in orientation or systematically rotated with occasionally unexpected rotations. At the single neuron and population level, there was significantly enhanced orientation-selective response to unexpected visual stimuli through a boost in gain, which was prominent in awake mice but also present to a lesser extent under anesthesia. We implemented a computational model to demonstrate how neuronal responses were best characterized when adaptation and expectation parameters were combined. Our results demonstrated that adaptation and prediction have unique signatures on activity of V1 neurons.

Download Full-text

Emergent orientation selectivity from random networks in mouse visual cortex

10.1101/285197 ◽

2018 ◽

Author(s):

J.J. Pattadkal ◽

G. Mato ◽

C. van Vreeswijk ◽

N. J. Priebe ◽

D. Hansel

Keyword(s):

Visual Cortex ◽

Calcium Imaging ◽

Receptive Fields ◽

Orientation Selectivity ◽

Random Networks ◽

Two Dimensional ◽

V1 Neurons ◽

Mouse Visual Cortex ◽

Whole Cell Recordings ◽

Random Connectivity

SummaryWe study the connectivity principles underlying the emergence of orientation selectivity in primary visual cortex (V1) of mammals lacking an orientation map. We present a computational model in which random connectivity gives rise to orientation selectivity that matches experimental observations. It predicts that mouse V1 neurons should exhibit intricate receptive fields in the two-dimensional frequency domain, causing shift in orientation preferences with spatial frequency. We find evidence for these features in mouse V1 using calcium imaging and intracellular whole cell recordings.

Download Full-text

Traumatic brain injury to primary visual cortex produces long-lasting circuit dysfunction

Communications Biology ◽

10.1038/s42003-021-02808-5 ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Jan C. Frankowski ◽

Andrzej T. Foik ◽

Alexa Tierno ◽

Jiana R. Machhor ◽

David C. Lyon ◽

...

Keyword(s):

Traumatic Brain Injury ◽

Visual Cortex ◽

Brain Injury ◽

Primary Visual Cortex ◽

Visual Stimuli ◽

Orientation Tuning ◽

V1 Neurons ◽

Adult Mice ◽

Electrophysiological Recordings

AbstractPrimary sensory areas of the mammalian neocortex have a remarkable degree of plasticity, allowing neural circuits to adapt to dynamic environments. However, little is known about the effects of traumatic brain injury on visual circuit function. Here we used anatomy and in vivo electrophysiological recordings in adult mice to quantify neuron responses to visual stimuli two weeks and three months after mild controlled cortical impact injury to primary visual cortex (V1). We found that, although V1 remained largely intact in brain-injured mice, there was ~35% reduction in the number of neurons that affected inhibitory cells more broadly than excitatory neurons. V1 neurons showed dramatically reduced activity, impaired responses to visual stimuli and weaker size selectivity and orientation tuning in vivo. Our results show a single, mild contusion injury produces profound and long-lasting impairments in the way V1 neurons encode visual input. These findings provide initial insight into cortical circuit dysfunction following central visual system neurotrauma.

Download Full-text

Pure tones modulate the representation of orientation and direction in the primary visual cortex

Journal of Neurophysiology ◽

10.1152/jn.00069.2019 ◽

2019 ◽

Vol 121 (6) ◽

pp. 2202-2214 ◽

Cited By ~ 5

Author(s):

John P. McClure ◽

Pierre-Olivier Polack

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulus ◽

Visual Stimuli ◽

Direction Selectivity ◽

Multimodal Integration ◽

Visual Responses ◽

V1 Neurons ◽

Pure Tones ◽

The Impact

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. Whereas multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. In the present study, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multimodal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue’s orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone. NEW & NOTEWORTHY The primary visual cortex (V1) receives direct inputs from the primary auditory cortex. Yet, the impact of sounds on visual processing in V1 remains controverted. We show that the modulation by pure tones of V1 visual responses depends on the orientation selectivity, direction selectivity, and response amplitudes of V1 neurons. Hence, audiovisual stimuli recruit a population of V1 neurons better tuned to the orientation and direction of the visual stimulus than unimodal visual stimuli.

Download Full-text

Continuous multiplexed population representations of task context in the mouse primary visual cortex

10.1101/2021.04.20.440666 ◽

2021 ◽

Author(s):

Marton Albert Hajnal ◽

Duy Tran ◽

Michael Einstein ◽

Mauricio Vallejo Martelo ◽

Karen Safaryan ◽

...

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Activity Patterns ◽

Visual Stimuli ◽

Stimulus Onset ◽

Decision Task ◽

Cognitive Variables ◽

Task Context ◽

Population Activity ◽

V1 Neurons

Primary visual cortex (V1) neurons integrate motor and multisensory information with visual inputs during sensory processing. However, whether V1 neurons also integrate and encode higher-order cognitive variables is less understood. We trained mice to perform a context-dependent cross-modal decision task where the interpretation of identical audio-visual stimuli depends on task context. We performed silicon probe population recordings of neuronal activity in V1 during task performance and showed that task context (whether the animal should base its decision on visual or auditory stimuli) can be decoded during both intertrial intervals and stimulus presentations. Context and visual stimuli were represented in overlapping populations but were orthogonal in the population activity space. Context representation was not static but displayed distinctive dynamics upon stimulus onset and offset. Thus, activity patterns in V1 independently represent visual stimuli and cognitive variables relevant to task execution.

Download Full-text

In Vivo Two-Photon Ca2+ Imaging Reveals Selective Reward Effects on Stimulus-Specific Assemblies in Mouse Visual Cortex

Journal of Neuroscience ◽

10.1523/jneurosci.1341-12.2013 ◽

2013 ◽

Vol 33 (28) ◽

pp. 11540-11555 ◽

Cited By ~ 32

Author(s):

P. M. Goltstein ◽

E. B. J. Coffey ◽

P. R. Roelfsema ◽

C. M. A. Pennartz

Keyword(s):

Visual Cortex ◽

Two Photon ◽

Mouse Visual Cortex ◽

Reward Effects

Download Full-text

Mouse visual cortex contains a region of enhanced spatial resolution

Nature Communications ◽

10.1038/s41467-021-24311-5 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Enny H. van Beest ◽

Sreedeep Mukherjee ◽

Lisa Kirchberger ◽

Ulf H. Schnabel ◽

Chris van der Togt ◽

...

Keyword(s):

Visual Cortex ◽

Eye Movements ◽

Visual Processing ◽

Receptive Fields ◽

Single Neurons ◽

Two Photon ◽

Representation Of Space ◽

Freely Moving ◽

Mapping Techniques ◽

Mouse Visual Cortex

AbstractThe representation of space in mouse visual cortex was thought to be relatively uniform. Here we reveal, using population receptive-field (pRF) mapping techniques, that mouse visual cortex contains a region in which pRFs are considerably smaller. This region, the “focea,” represents a location in space in front of, and slightly above, the mouse. Using two-photon imaging we show that the smaller pRFs are due to lower scatter of receptive-fields at the focea and an over-representation of binocular regions of space. We show that receptive-fields of single-neurons in areas LM and AL are smaller at the focea and that mice have improved visual resolution in this region of space. Furthermore, freely moving mice make compensatory eye-movements to hold this region in front of them. Our results indicate that mice have spatial biases in their visual processing, a finding that has important implications for the use of the mouse model of vision.

Download Full-text

In vivo two-photon imaging analysis of development of direction and orientation selectivity in the mouse visual cortex

Neuroscience Research ◽

10.1016/j.neures.2011.07.1122 ◽

2011 ◽

Vol 71 ◽

pp. e257

Author(s):

Madoka Narushima ◽

Nathalie L. Rochefort ◽

Christine Grienberger ◽

Nima Marandi ◽

Arthur Konnerth

Keyword(s):

Visual Cortex ◽

Orientation Selectivity ◽

Imaging Analysis ◽

Two Photon ◽

Photon Imaging ◽

Two Photon Imaging ◽

Mouse Visual Cortex

Download Full-text

Developmental dynamics of cross-modality in mouse visual cortex

10.1101/150847 ◽

2017 ◽

Cited By ~ 1

Author(s):

Ryoma Hattori ◽

Takao K Hensch

Keyword(s):

Visual Cortex ◽

Orientation Selectivity ◽

Functional Roles ◽

V1 Neurons ◽

Auditory Responses ◽

Functional Maturation ◽

Dark Exposure ◽

Genetic Deletion ◽

Mouse Visual Cortex ◽

Developmental Dynamics

SUMMARYMaturation of GABAergic circuits in primary visual cortex (V1) opens a critical period (CP), a developmental window of enhanced plasticity for visual functions. However, how inhibition promotes the plasticity remains unclear. Here, we investigated the developmental dynamics of auditory responses and audiovisual interactions in mouse V1. Modulation of V1 spiking activity by a transient sound was temporally dynamic with alternating enhancement and suppression phases. When paired with grating visual stimuli, sound-driven spike enhancement and suppression were weaker and stronger with preferred orientation than with non-preferred orientations, respectively, leading to impaired net orientation selectivity in V1 neurons. Strikingly, the net orientation selectivity was impervious to sound specifically during the CP due to equal total amounts of sound-driven spike enhancements and suppressions. This balance of spike modulations at the CP was achieved by the preferential maturation of sound-driven spike suppression. However, further maturation of sound-driven spike enhancement broke the balance after the CP. Spectral analysis of field potentials revealed the enhancement of a GABA-mediated sound-driven power suppression specifically at CP. Reduction of inhibition by 10-day dark-exposure or genetic deletion of GAD65 gene dampened sound-driven spike suppression in V1. Furthermore, acute suppression of either parvalbumin-expressing (PV) or somatostatinexpressing (SST) neurons suggested their early or late recruitments by sound, respectively. Our results point to the dampened net non-visual sensory influence as one of the functional roles of GABA circuit maturation during a developmental CP. The insensitivity of visual selectivity to sound during the CP may promote functional maturation of V1 as visual cortex.

Download Full-text