Identification of a Brainstem Circuit Regulating Visual Cortical State in Parallel with Locomotion (original) (raw)
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Locomotion in vertebrates relies on high brain centers converging onto the mesencephalic locomotor region (MLR). How the MLR recruits brainstem reticulospinal neurons (RSNs) to initiate locomotion is incompletely understood due to the challenge of recording these cells in vivo. To tackle this question, we leveraged the transparency and genetic accessibility of larval zebrafish. In this model organism, we uncovered the locus of the MLR as a small region dorsal to the locus coeruleus containing glutamatergic and cholinergic neurons. MLR stimulations reliably elicited forward bouts of controlled duration and speed. We find that the MLR elicits forward locomotion by recruiting V2a RSNs in the pontine and retropontine regions, and gradually in the medulla. Remarkably, recruited V2a RSNs in the medulla act as maintain cells encoding speed of forward locomotion. Altogether, our study reveals that the MLR recruits genetically-identified reticulospinal neurons in the medulla to control the k...
Locomotion modulates specific functional cell types in the mouse visual thalamus
The visual system is composed of diverse cell types that encode distinct aspects of the visual scene and may form separate processing channels. Here we present further evidence for that hypothesis whereby functional cell groups in the dorsal lateral geniculate nucleus (dLGN) are differentially modulated during behavior. Using simultaneous multi-electrode recordings in dLGN and primary visual cortex (V1) of behaving mice, we characterized the impact of locomotor activity on response amplitude, variability, correlation and spatiotemporal tuning. Locomotion strongly impacts the amplitudes of dLGN and V1 responses but the effects on variability and correlations are relatively minor. With regards to tunings, locomotion enhances dLGN responses to high temporal frequencies, preferentially affecting ON transient cells and neurons with nonlinear responses to high spatial frequencies. Channel specific modulations may serve to highlight particular visual inputs during active behaviors.
Vision and locomotion shape the interactions between neuron types in mouse visual cortex
2016
SummaryIn the mouse primary visual cortex (V1), sensory responses are shaped by behavioral factors such as locomotion. These factors are thought to control a disinhibitory circuit, whereby interneurons expressing vasoactive intestinal peptide (Vip) inhibit those expressing somatostatin (Sst), disinhibiting pyramidal cells (Pyr). We measured the effect of locomotion on these neurons and on interneurons expressing parvalbumin (Pvalb) in layer 2/3 of mouse V1, and found in-consistencies with the disinhibitory model. In the presence of large stimuli, locomotion increased Sst cell responses without suppressing Vip cells. In the presence of small stimuli, locomotion increased Vip cell responses without suppressing Sst cells. A circuit model could reproduce each cell type’s activity from the measured activity of other cell types, but only if we allowed locomotion to increase feedforward synaptic weights while modulating recurrent weights. These results suggest that locomotion alters cortic...
Formation and function of neural circuits underlying visual and locomotor behaviors
2013
Overview: In this last part of the course, we focus on the formation and function of neural circuits underlying visual and locomotor behaviors. It is therefore important to ask: What are the advantages of zebrafish for studies of neuronal circuits and behavior? the transparency of the embryo and larvae, which has made them so useful in screening for developmental defects, also allows for optical studies of their neuronal circuits. the simplicity of the nervous system (compared to other vertebrate model systems) and the detailed maps of identified spinal cord and hindbrain neurons allow the study of circuits and behavior at a single cell resolution. -the extrauterine development facilitates a number of powerful techniques, including single cell recording, labeling of individual neurons and their projections, application of drugs, and lesion experiments using sharp needles or a laser beam. the development of genetic constructs such as channelrhodopsin and halorhodopsin allow for optic...
Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex
Neuron, 2010
Studies of visual processing in rodents have conventionally been performed in anesthetized animals, precluding examination of the effects of behavior on visually-evoked responses. We have now studied the response properties of neurons in primary visual cortex of awake mice that were allowed to run on a freely rotating spherical treadmill with their heads fixed. Most neurons showed more than a doubling of visually-evoked firing rate as the animal transitioned from standing still to running, without changes in spontaneous firing or stimulus selectivity. Tuning properties in the awake animal were similar to those measured previously in anesthetized animals. Response magnitude in the lateral geniculate nucleus did not increase with locomotion, demonstrating that the striking change in responsiveness did not result from peripheral effects at the eye. Interestingly, some narrow-spiking cells were spontaneously active during running but suppressed by visual stimuli. These results demonstrate powerful cell type-specific modulation of visual processing by behavioral state in awake mice.
The influence of locomotion on sensory processing and its underlying neuronal circuits
e-Neuroforum, 2018
Processing of sensory information can be modulated in both cortex and thalamus by behavioral context, such as locomotion. During active behaviors, coding of sensory stimuli and perception are improved, in particular during physical activity of moderate intensity. These locomotion-related modulations seem to arise from a combination of mechanisms, including neuromodulation, the recruitment of inhibitory interneurons, and specific top-down or motor-related inputs. The application of new experimental methods in mice during walking under head-fixation on treadmills made it possible to study the circuit and cellular basis underlying modulations by behavioral context with unprecedented detail. This article reviews the current state of these studies and highlights some important open questions.
The coupling of vision with locomotion in cortical blindness
Vision Research, 2014
Maintaining or modifying the speed and direction of locomotion requires the coupling of the locomotion with the retinal optic flow that it generates. It is shown that this essential behavioral capability, which requires on-line neural control, is preserved in the cortically blind hemifield of a hemianope. In experiments, optic flow stimuli were presented to either the normal or blind hemifield while the patient was walking on a treadmill. Little difference was found between the hemifields with respect to the coupling (i.e. co-dependency) of optic flow detection with locomotion. Even in the cortically blind hemifield, faster walking resulted in the perceptual slowing of detected optic flow, and self-selected locomotion speeds demonstrated behavioral discrimination between different optic flow speeds. The results indicate that the processing of optic flow, and thereby on-line visuo-locomotor coupling, can take place along neural pathways that function without processing in Area V1, and thus in the absence of conscious intervention. These and earlier findings suggest that optic flow and object motion are processed in parallel along with correlated non-visual locomotion signals. Extrastriate interactions may be responsible for discounting the optical effects of locomotion on the perceived direction of object motion, and maintaining visually guided self-motion.
The opto-locomotor reflex as a tool to measure sensitivity to moving random dot patterns in mice
Scientific Reports, 2018
We designed a method to quantify mice visual function by measuring reflexive opto-locomotor responses. Mice were placed on a Styrofoam ball at the center of a large dome on the inside of which we projected moving random dot patterns. Because we fixed the heads of the mice in space and the ball was floating on pressurized air, locomotion of the mice was translated to rotation of the ball, which we registered. Sudden onsets of rightward or leftward moving patterns caused the mice to reflexively change their running direction. We quantified the opto-locomotor responses to different pattern speeds, luminance contrasts, and dot sizes. We show that the method is fast and reliable and the magnitude of the reflex is stable within sessions. We conclude that this opto-locomotor reflex method is suitable to quantify visual function in mice. In recent years, mice have become an important animal model for studies on visual processing. Although mice rely much less on vision than primates, their visual system largely resembles that of higher mammals 1-4. Moreover, mice offer unique opportunities to study the functional circuitry of vision. For example, through the invention of genetically encoded calcium current and voltage indicators it is possible to record in parallel the activity of hundreds of neurons in cortex in the behaving mouse 5-10. The activity of large groups of neurons can be altered by applying optogenetics 11-14 or activated by designer drugs 15,16. These neurophysiological techniques offer the opportunity to directly relate neuronal function in retina and visual cortex to visually driven behaviour 2,17-20. For this purpose, suitable tests of visual function are needed. Over the years many behavioural tests for mouse visual function have been developed 21-23. Visual function in mice is traditionally tested with simple behavioural paradigms based on reflexes, such as the eye blink reflex, the pupil light response 21,24 , light-dark transition test 25 and optokinetic reflexive responses of the eye or the head to large moving patterns 26-29. These reflexes are thought to rely on the retino-tectal pathway, which is strongly developed in the mouse 30-32. Higher perceptual facilities (pattern, depth, orientation) are thought to rely more on retino-cortical pathways. Examples of tests that probe these are the visual cliff test 33 and modified Morris water maze tests 34-37. Many recent studies of mouse visual perception rely on fixating the head in space. This has the advantage of increased control over the visual stimulation and it provides the stability that is typically required in neural techniques such as two-photon calcium imaging 20,38,39 and single unit or patch-clamp recording 40,41. Perceptual tasks that head-fixed mice perform concurrently with these neurophysiological assays typically involve licking responses or lever presses to visual stimuli according to specific, trained rules of varying complexity 21,40,42-47. The purpose of this study is to test a method we developed that leverages the opto-locomotor reflex (OLR) in a head-fixed paradigm. This reflex effectively stabilises whole-scene motion by cancelling it with a body orienting movement of the same magnitude 46-50. In this study, we fixed mice with their heads over the center of a spherical, 2D treadmill. All mice spontaneously started running forward. The treadmill was located at the center of a 112 cm dome on the inside of which we projected moving random dot patterns. The presentation of rightward or leftward moving patterns caused the mice to reflexively change their running direction. We quantified the
Optogenetic Activation of A11 Region Increases Motor Activity
Frontiers in neural circuits, 2018
Limbic brain regions drive goal-directed behaviors. These behaviors often require dynamic motor responses, but the functional connectome of limbic structures in the diencephalon that control locomotion is not well known. The A11 region, within the posterior diencephalon has been postulated to contribute to motor function and control of pain. Here we show that the A11 region initiates movement. Photostimulation of channelrhodopsin 2 (ChR2) transfected neurons in A11 slice preparations showed that neurons could follow stimulation at frequencies of 20 Hz. Our data show that photostimulation of ChR2 transfected neurons in the A11 region enhances motor activity often leading to locomotion. Using vGluT2-reporter and vGAT-reporter mice we show that the A11 tyrosine hydroxylase positive (TH) dopaminergic neurons are vGluT2 and vGAT negative. We find that in addition to dopaminergic neurons within the A11 region, there is another neuronal subtype which expresses the monoenzymatic aromatic L-...