scholarly journals Optogenetic suppression of corticogeniculate feedback in anesthetized ferrets is overridden by visual stimulation

2021 ◽  
Author(s):  
Silei Zhu ◽  
J. Michael Hasse ◽  
Farran Briggs

The feedforward projection from the retina shapes the spatial receptive field properties of neurons in the dorsal lateral geniculate nucleus of the thalamus (LGN). Corticogeniculate feedback from the visual cortex appears to exert a more subtle, modulatory influence on LGN responses. Studies involving manipulations of corticogeniculate feedback have yielded inconsistent findings, but the reasons for these inconsistencies are not known. To examine the functional contributions of corticogeniculate feedback, and to resolve past inconsistencies, we examined the effects of selective optogenetic suppression of corticogeniculate neurons in anesthetized ferrets. In particular, we examined the responses of LGN and V1 neurons during optogenetic suppression of corticogeniculate feedback in the presence and absence of visual stimulation and across conditions in which the frequency of LED illumination varied. Optogenetic suppression of corticogeniculate feedback decreased activity among LGN neurons in the absence of visual stimulation, dispelling the notion that anesthesia causes a floor effect. In contrast, suppressing corticogeniculate feedback did not affect the visual responses of LGN neurons, suggesting that feedforward visual stimulus drive overrides weak corticogeniculate influence. Optogenetic effects on LGN and V1 neuronal responses depended on the frequency of LED illumination, with higher frequency illumination inducing slow oscillations in V1, dis-inhibiting V1 neurons locally, and producing more suppression among LGN neurons. These results demonstrate that corticogeniculate influence depends on stimulation parameters including visual stimulus conditions and frequency of inactivation. Furthermore, weak corticogeniculate influence is overridden by strong feedforward visual stimulus drive; this attribute is the most likely source of inconsistencies in past studies.

1998 ◽  
Vol 15 (4) ◽  
pp. 711-729 ◽  
Author(s):  
KLAUS FUNKE ◽  
ULF T. EYSEL

Action potentials of single perigeniculate (PGN) cells and relay cells of the dorsal lateral geniculate nucleus (dLGN) with topographically matched or at least partially overlapping receptive fields (RF) were simultaneously recorded in the anesthetized and paralyzed cat during visual stimulation with moving gratings or flashing light spots of different size. In many cases, PGN cells showed an activity pattern which appeared like a mirror image of distinct periods of dLGN activity. Flashing spots evoked transient volleys of activity in PGN cells which increased in strength and shortened in latency with increasing size of the stimulus. These responses were temporally matched with inhibitory phases in the early part of visual responses in the dLGN. The spatio-temporal properties of the RFs were established by reverse correlation of the spike activity with the spatially random presentation of bright and dark spots within an array of 20 × 20 positions. Anticorrelated firing patterns of such kind could also be elicited as interocular inhibition with stimulation of the perigeniculate RF in the nondominant eye. Inversely correlated changes in spontaneous and visually induced activity were also visible during spontaneous changes in EEG pattern. With increasing synchronization of the EEG (predominance of delta-waves) the strength of geniculate visual responses declined while maintained perigeniculate activity increased. A weakened interocular and monocular inhibition of dLGN relay cells during visual stimulation of PGN RFs could be achieved with local reversible inactivation of PGN areas topographically matched with the dLGN recording sites. The results indicate that the PGN contributes to the state-dependent control of retino-geniculate transmission and to the monocular and interocular inhibitory processes that shape the visual responses in the dLGN.


2019 ◽  
Vol 121 (6) ◽  
pp. 2202-2214 ◽  
Author(s):  
John P. McClure ◽  
Pierre-Olivier Polack

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.


1996 ◽  
Vol 76 (5) ◽  
pp. 2907-2918 ◽  
Author(s):  
M. Schmidt

1. Neurons in the pretectal nuclear complex that project to the ipsilateral dorsal lateral geniculate nucleus (LGNd) were identified by antidromic activation after electrical LGNd stimulation in awake cats, and their response properties were characterized to retinal image shifts elicited either by external visual stimulus movements or during spontaneous saccadic eye movements on a stationary visual stimulus, and to saccades in darkness. Eye position was monitored with the use of a scleral search coil and care was taken to assure stability of the eyes during presentation of moving visual stimuli. 2. Of a total sample of 134 cells recorded, 27 neurons were antidromically activated by electrical LGNd stimulation. In addition, responses from neurons that were not activated from the LGNd were also analyzed, including 19 “retinal slip” cells, which selectively respond to slow horizontal stimulus movements, and 21 “jerk” cells, which are specifically activated by rapid stimulus shifts. All recorded neurons were located in the nucleus of the optic tract and in the posterior pretectal nucleus. 3. In the light, neurons identified as projecting to the LGNd responded maximally to saccadic eye movements and to externally generated sudden shifts of large visual stimuli. Slow stimulus drifts did not activate these neurons. Response latencies were shorter and peak activities were increased during saccades compared with pure visual stimulation. No systematic correlation between response latency, response duration, or the number of spikes in the response and saccade direction, saccade amplitude, or saccade duration was found. Saccades and rapid stimulus shifts in the light also activated jerk cells but not retinal slip cells. 4. All 27 antidromically activated neurons also responded to spontaneous saccadic eye movements in complete darkness. Responses to saccades in the dark, however, had longer response latencies and lower peak activities than responses to saccades in light. As in the light, response parameters in darkness seemed not to code specific saccade parameters. Cells that were not activated from LGNd were found to be unresponsive to saccades in the dark. 5. According to their specific activation by saccades in darkness, LGNd-projecting pretectal neurons are termed “saccade neurons” to distinguish them from other pretectal cell populations, in particular from jerk neurons, which show similar response properties in light. 6. The saccade-related activation of pretectal saccade neurons may be used to modulate visual responses of LGNd relay cells following saccadic eye movements. Because the pretectogeniculate projection in cat most likely is GABAergic and terminates on inhibitory LGNd interneurons, its activation may lead to a saccade-locked disinhibition of relay cells. This input could counter the strong inhibition induced in the LGNd after shifts of gaze direction and lead to a resetting of LGNd cell activity.


1990 ◽  
Vol 63 (3) ◽  
pp. 523-538 ◽  
Author(s):  
R. Lal ◽  
M. J. Friedlander

1. The nature and time window of interaction between passive phasic eye movement signals and visual stimuli were studied for dorsal lateral geniculate nucleus (LGNd) neurons in the cat. Extracellular recordings were made from single neurons in layer A of the left LGNd of anesthetized paralyzed cats in response to a normalized visual stimulus presented to the right eye at each of several times of movement of the left eye. The left eye was moved passively at a fixed amplitude and velocity while varying the movement onset time with respect to the visual stimulus onset in a randomized and interleaved fashion. Visual stimuli consisted of square-wave modulated circular spots of appropriate contrast, sign, and size to elicit an optimal excitatory response when placed in the neurons' receptive-field (RF) center. 2. Interactions were analyzed for 78 neurons (33 X-neurons, 43 Y-neurons, and 2 physiologically unclassified neurons) on 25-65 trials of identical visual stimuli for each of eight times of eye movement. 3. Sixty percent (47/78) of the neurons tested had a significant eye movement effect (ANOVA, P less than 0.05) on some aspect of their visual response. Of these 47 neurons, 42 (89%) had a significant (P less than 0.05) effect of an appropriately timed eye movement on the number of action potentials, 36 (77%) had a significant effect on the mean peak firing rate, and 31 (66%) were significantly affected as evaluated by both criteria. 4. The eye movement effect on the neurons' visual responses was primarily facilitatory. Facilitation was observed for 37 (79%) of the affected neurons. For 25 of these 37 neurons (68%), the facilitation was significant (P less than 0.05) as evaluated by both criteria (number of action potentials and mean peak firing rate). Ten (21%) of the affected neurons had their visual response significantly inhibited (P less than 0.05). 5. Sixty percent (46/78) of the neurons were tested for the effect of eye movement on both visually elicited activity (visual stimulus contrast = 2 times threshold) and spontaneous activity (contrast = 0). Eye movement significantly affected the visual response of 23 (50%) of these neurons. However, spontaneous activity was significantly affected for only nine (20%) of these neurons. The interaction of the eye movement and visual signals was nonlinear. 6. Nine of 12 neurons (75%) tested had a directionally selective effect of eye movement on the visual response, with most (8/9) preferring the temporal ward direction.(ABSTRACT TRUNCATED AT 400 WORDS)


2015 ◽  
Vol 114 (2) ◽  
pp. 1172-1182 ◽  
Author(s):  
Carl R. Stoelzel ◽  
Joseph M. Huff ◽  
Yulia Bereshpolova ◽  
Jun Zhuang (庄骏) ◽  
Xiaojuan Hei (黑晓娟) ◽  
...  

Sensory adaptation serves to adjust awake brains to changing environments on different time scales. However, adaptation has been studied traditionally under anesthesia and for short time periods. Here, we demonstrate in awake rabbits a novel type of sensory adaptation that persists for >1 h and acts on visual thalamocortical neurons and their synapses in the input layers of the visual cortex. Following prolonged visual stimulation (10–30 min), cells in the dorsal lateral geniculate nucleus (LGN) show a severe and prolonged reduction in spontaneous firing rate. This effect is bidirectional, and prolonged visually induced response suppression is followed by a prolonged increase in spontaneous activity. The reduction in thalamic spontaneous activity following prolonged visual activation is accompanied by increases in 1) response reliability, 2) signal detectability, and 3) the ratio of visual signal/spontaneous activity. In addition, following such prolonged activation of an LGN neuron, the monosynaptic currents generated by thalamic impulses in layer 4 of the primary visual cortex are enhanced. These results demonstrate that in awake brains, prolonged sensory stimulation can have a profound, long-lasting effect on the information conveyed by thalamocortical inputs to the visual cortex.


Author(s):  
Aleena R. Garner ◽  
Georg B. Keller

AbstractLearned associations between stimuli in different sensory modalities can shape the way we perceive these stimuli. However, it is not well understood how these interactions are mediated or at what level of the processing hierarchy they occur. Here we describe a neural mechanism by which an auditory input can shape visual representations of behaviorally relevant stimuli through direct interactions between auditory and visual cortices in mice. We show that the association of an auditory stimulus with a visual stimulus in a behaviorally relevant context leads to experience-dependent suppression of visual responses in primary visual cortex (V1). Auditory cortex axons carry a mixture of auditory and retinotopically matched visual input to V1, and optogenetic stimulation of these axons selectively suppresses V1 neurons that are responsive to the associated visual stimulus after, but not before, learning. Our results suggest that cross-modal associations can be communicated by long-range cortical connections and that, with learning, these cross-modal connections function to suppress responses to predictable input.


1995 ◽  
Vol 12 (1) ◽  
pp. 21-33 ◽  
Author(s):  
Klaus Funke ◽  
Ulf T. Eysel

AbstractThe modulatory influence of pretectal neurons on retino-geniculate transmission in the cat was studied by cross-correlation analysis of single-unit activity simultaneously recorded from the dorsal lateral geniculate nucleus (dLGN) and the pretectum (PT) and with reversible inactivation of the PT by GABA microiontophoresis during simultaneous visual stimulation of PT and dLGN neurons. Visually induced population activity in PT nuclei was achieved by a moving (or counterphasing) grating which was presented in the background of the light spot used to stimulate the dLGN neuron. As a control, the light spot was presented on a stationary grating to avoid stimulation of PT neurons but to yield the same illumination of the background. Extracellularly recorded dLGN relay cells of the X- and Y-type were found to be differentially affected by the PT-dLGN projection. During visual stimulation of PT cells, X cells were strongly inhibited and this effect was significantly reduced during PT inactivation. By contrast, the visual responses of most Y cells were affected neither by PT stimulation nor by PT inactivation. In addition, the temporal structure of spike patterns during the light response was examined with autocorrelograms and spike-interval distributions. X-on cells often exhibited a multimodal interval distribution and oscillatory type of activity. During stimulation of the PT interval distributions changed in a characteristic manner and oscillations disappeared. Both effects could be almost totally cancelled by PT inactivation. By contrast, the temporal structure of Y-cell responses was not affected. Our results demonstrate for the first time a pretectal modulation of retino-geniculate transmission in cat dLGN which is clearly different for X and Y cells. This influence seems to be mediated via (inhibitory) interneurons, since we found no indication for a direct coupling between PT and dLGN units. This projection might contribute to the well-known phenomenon of saccadic suppression.


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