Hippocampal representation of touch and sound guided behavior (original) (raw)
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Auditory stimuli elicit hippocampal neuronal responses during sleep
To investigate how hippocampal neurons code behaviorally salient stimuli, we recorded from neurons in the CA1 region of hippocampus in rats while they learned to associate the presence of sound with water reward. Rats learned to alternate between two reward ports at which, in 50% of the trials, sound stimuli were presented followed by water reward after a 3-s delay. Sound at the water port predicted subsequent reward delivery in 100% of the trials and the absence of sound predicted reward omission. During this task, 40% of recorded neurons fired differently according to which of the two reward ports the rat was visiting. A smaller fraction of neurons demonstrated onset response to sound/nosepoke (19%) and reward delivery (24%). When the sounds were played during passive wakefulness, 8% of neurons responded with short latency onset responses; 25% of neurons responded to sounds when they were played during sleep. During sleep the short-latency responses in hippocampus are intermingled with long lasting responses which in the current experiment could last for 1–2 s. Based on the current findings and the results of previous experiments we described the existence of two types of hippocampal neuronal responses to sounds: sound-onset responses with very short latency and longer-lasting sound-specific responses that are likely to be present when the animal is actively engaged in the task.
PLoS ONE, 2011
Understanding the mechanisms by which sensory experiences are stored remains a compelling challenge for neuroscience. Previous work has described how the activity of neurons in the sensory cortex allows rats to discriminate the physical features of an object contacted with their whiskers. But to date there is no evidence about how neurons represent the behavioural significance of tactile stimuli, or how they are encoded in memory. To investigate these issues, we recorded single-unit firing and local field potentials from the CA1 region of hippocampus while rats performed a task in which tactile stimuli specified reward location. On each trial the rat touched a textured plate with its whiskers, and then turned towards the Left or Right water spout. Two textures were associated with each reward location. To determine the influence of the rat's position on sensory coding, we placed it on a second platform in the same room where it performed the identical texture discrimination task. Over 25 percent of the sampled neurons encoded texture identity -their firing differed for two stimuli associated with the same reward location -and over 50 percent of neurons encoded the reward location with which the stimuli were associated. The neuronal population carried texture and reward location signals continuously, from the moment of stimulus contact until the end of reward collection. The set of neurons discriminating between one texture pair was found to be independent of, and partially overlapping, the set of neurons encoding the discrimination between a different texture pair. In a given neuron, the presence of a tactile signal was uncorrelated with the presence, magnitude, or timing of reward location signals. These experiments indicate that neurons in CA1 form a texture representation independently of the action the stimulus is associated with and retain the stimulus representation through reward collection.
Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task
Journal of Neurophysiology, 2012
Itskov PM, Vinnik E, Honey C, Schnupp J, Diamond ME. Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task. To investigate how hippocampal neurons encode sound stimuli, and the conjunction of sound stimuli with the animal's position in space, we recorded from neurons in the CA1 region of hippocampus in rats while they performed a sound discrimination task. Four different sounds were used, two associated with water reward on the right side of the animal and the other two with water reward on the left side. This allowed us to separate neuronal activity related to sound identity from activity related to response direction. To test the effect of spatial context on sound coding, we trained rats to carry out the task on two identical testing platforms at different locations in the same room. Twenty-one percent of the recorded neurons exhibited sensitivity to sound identity, as quantified by the difference in firing rate for the two sounds associated with the same response direction. Sensitivity to sound identity was often observed on only one of the two testing platforms, indicating an effect of spatial context on sensory responses. Forty-three percent of the neurons were sensitive to response direction, and the probability that any one neuron was sensitive to response direction was statistically independent from its sensitivity to sound identity. There was no significant coding for sound identity when the rats heard the same sounds outside the behavioral task. These results suggest that CA1 neurons encode sound stimuli, but only when those sounds are associated with actions. episodic memory; systems neuroscience; interneurons; auditory objects; pyramidal cells; electrophysiology; mutual information; sensory representation * P. M. Itskov and E. Vinnik contributed equally to this work.
The robot vibrissal system: Understanding mammalian sensorimotor co-ordination through biomimetics
We consider the problem of sensorimotor coordination in mammals through the lens of vibrissal touch, and via the methodology of embodied computational neuroscience—using biomimetic robots to synthesize and investigate models of mammalian brain architecture. The chapter focuses on five major brain subsystems and their likely role in vibrissal system function—superior colliculus, basal ganglia, somatosensory cortex, cerebellum, and hippocampus. With respect to each of these we demonstrate how embodied modelling has helped elucidate their likely function in the brain of awake behaving animals. We also demonstrate how the appropriate coordination of these subsystems , with a model of brain architecture, can give rise to integrated behaviour in a lifelike whiskered robot.
Special issue: Review Limbic systems for emotion and for memory, but no single limbic system
Emotion Cingulate cortex Amygdala Episodic memory Hippocampus Reward value a b s t r a c t The concept of a (single) limbic system is shown to be outmoded. Instead, anatomical, neurophysiological, functional neuroimaging, and neuropsychological evidence is described that anterior limbic and related structures including the orbitofrontal cortex and amygdala are involved in emotion, reward valuation, and reward-related decision-making (but not memory), with the value representations transmitted to the anterior cingulate cortex for actioneoutcome learning. In this 'emotion limbic system' a computational principle is that feedforward pattern association networks learn associations from visual, olfactory and auditory stimuli, to primary reinforcers such as taste, touch, and pain. In primates including humans this learning can be very rapid and rule-based, with the orbitofrontal cortex overshadowing the amygdala in this learning important for social and emotional behaviour. Complementary evidence is described showing that the hippocampus and limbic structures to which it is connected including the posterior cingulate cortex and the fornix-mammillary body-anterior thalamus-posterior cingulate circuit are involved in episodic or event memory, but not emotion. This 'hippocampal system' receives information from neocortical areas about spatial location, and objects, and can rapidly associate this information together by the different computational principle of autoassociation in the CA3 region of the hippocampus involving feedback. The system can later recall the whole of this information in the CA3 region from any component, a feedback process, and can recall the information back to neocortical areas, again a feedback (to neocortex) recall process. Emotion can enter this memory system from the orbitofrontal cortex etc., and be recalled back to the orbitofrontal cortex etc. during memory recall, but the emotional and hippocampal networks or 'limbic systems' operate by different computational principles, and operate independently of each other except insofar as an emotional state or reward value attribute may be part of an episodic memory. ª
State-dependencies of learning across brain scales
Frontiers in computational neuroscience, 2015
Learning is a complex brain function operating on different time scales, from milliseconds to years, which induces enduring changes in brain dynamics. The brain also undergoes continuous "spontaneous" shifts in states, which, amongst others, are characterized by rhythmic activity of various frequencies. Besides the most obvious distinct modes of waking and sleep, wake-associated brain states comprise modulations of vigilance and attention. Recent findings show that certain brain states, particularly during sleep, are essential for learning and memory consolidation. Oscillatory activity plays a crucial role on several spatial scales, for example in plasticity at a synaptic level or in communication across brain areas. However, the underlying mechanisms and computational rules linking brain states and rhythms to learning, though relevant for our understanding of brain function and therapeutic approaches in brain disease, have not yet been elucidated. Here we review known mec...
Brain research. Cognitive brain research, 2002
This review explores the roles of several sensory modalities in the establishment and maintenance of discharges correlated with head position and orientation in neurons of the hippocampus and associated structures in the Papez circuit. Focus is placed on the integration of signals related to environmental cues and to displacement movements, both of external and internal origin. While the visual, vestibular and motor systems each exert influences, position and head direction signals are nevertheless maintained in the absence of any one of these respective inputs. Context-related changes in hippocampal discharge correlates are also highlighted. These characteristics provide these signals with robustness and flexibility, properties particularly suited for cognitive processes such as contextual processing, memory and planning.
Mnemonic information in the rodent hippocampus during wake and sleep states
2002
To investigate the representation of information in the hippocampus during memory processes, we simultaneously monitored the spiking activity of many single neurons in freely behaving rats during spatial locomotor tasks and periods of sleep. The first experiment examined the effect of differential reinforcement on the hippocampal representation of space, as mediated by the spatial receptive fields, or place fields, of hippocampal pyramidal neurons.
Spatial navigation in geometric mazes: A computational model of rodent behavior
Unpublished doctoral thesis, É cole Polytechnique …, 2007
Navigation is defined as the capability of planning and performing a path from the current position towards a desired location. Different types, or strategies, of navigation are used by animals depending on the task they are trying to solve. Visible goals can be approached directly, while navigation to a hidden goal usually requires a memorized representation of relative positions of the goal and surrounding landmarks.