The standard framework of hippocampal memory function states that CA3 serves as a Hopfield type auto-associative memory that stores patterns in its recurrent connections. Dentate gyrus orthogonalizes patterns and prepares them for storage in CA3. CA1 helps decoding patterns from CA3.

The CRISP theory recently proposed by Sen Cheng states that the main site of storage are not the recurrent connections in CA3 but the feed-forward connections to and from CA1. CA3 serves as a sequence generator to which memory sequences are associated.

I present here some simulation results that investigate the implications of the CRISP theory and support the idea that storage in feed-forward connections might have computational advantages over the standard view of storage in recurrent connections in CA3.

Hippocampal place cell ensembles form a cognitive map of space during exposure to novel environments. However, surprisingly little evidence exists to support the idea that synaptic plasticity in place cells is involved in forming new place fields. Here we used high-resolution functional imaging to determine the signaling patterns in CA1 soma, dendrites, and axons associated with place field formation when mice are exposed to novel virtual environments. We found that putative local dendritic spikes often occur prior to somatic place field firing. Subsequently, the first occurrence of somatic place field firing was associated with widespread regenerative dendritic events, which decreased in prevalence with increased novel environment experience. This transient increase in regenerative events was likely facilitated by a reduction in dendritic inhibition. Since regenerative dendritic events can provide the depolarization necessary for Hebbian potentiation, these results suggest that activity-dependent synaptic plasticity underlies the formation of many CA1 place fields.

Episodic memory is defined as memory for events occurring at a specific time and place. Neurophysiological recordings from brain regions in behaving rodents demonstrate neuronal response properties that may code space and time for episodic memory. This includes the coding in entorhinal cortex and hippocampus of spatial location by place cells (O'Keefe and Burgess, 1996) and grid cells (Hafting et al., 2005; Stensola et al., 2012). This talk will focus on data on the coding of temporal intervals by time cells (Kraus et al., 2013; 2015) of running speed by speed cells (Kropff et al., 2015; Hinman et al., 2016) and of environmental barriers by allocentric boundary cells (Solstad et al., 2008; Lever et al., 2009) as well as egocentric boundary cells (Hinman et al., 2017). Experimental data and computational modeling have explored potential cortical and subcortical mechanisms for the neural coding of time and space. Inactivation of input from the medial septum impairs the responses of neurons coding space (Brandon et al., 2011) and time (Wang et al., 2014) indicating subcortical contributions, but grid cells and boundary cells alter their coding in response to sensory input about environmental barriers conveyed by cortical inputs.

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Corticogeniculate circuits connect the primary visual cortex with the visual thalamus in the feedback direction and are a subset of corticothalamic circuits that are ubiquitous across mammals and sensory systems. Corticogeniculate feedback is anatomically robust in that the number of synapses onto thalamic relay neurons originating from the cortex far outnumber those originating from the retina. However, the functional role of corticogeniculate feedback in vision has remained a stubborn puzzle in visual neuroscience. We employed a novel combination of virus-mediated gene delivery and optogenetics to selectively and reversibly manipulate the activity of corticogeniculate neurons in vivo. We recorded the responses of thalamic neurons in response to visual stimulation with additional optogenetic activation of corticogeniculate feedback. We discovered that corticogeniculate feedback dramatically sharpens the response precision of visual thalamic neurons. Specifically, stimulation of corticogeniculate feedback reduced onset response latencies, increased spike timing precision, and reduced the size of the classical receptive field among thalamic neurons. We propose a simple circuit-based model to explain these effects. Together, our findings suggest that corticogeniculate feedback controls the timing of thalamic responses to visual stimuli and broadly support the notion that the thalamus is much more than a simple relay of sensory information.

Neural dynamics represent the hard-to-interpret substrate of circuit computations. Advances in large-scale recordings have highlighted the sheer spatiotemporal complexity of circuit dynamics, portraying in detail the difficulty of interpreting such dynamics and relating it to computation. Considering preparatory activity in a delayed response task we utilized neural recordings performed simultaneously with optogenetic perturbations to probe circuit dynamics. First, we revealed a surprising robustness in the detailed evolution of certain dimensions of the population activity, beyond what was thought to be the case experimentally and theoretically. Second, the robust dimension in activity space carries nearly all of the decodable behavioral information whereas other non-robust dimensions contained nearly no decodable information, consistent with the circuit being setup to make informative dimensions stiff, i.e., resistive to perturbations, leaving uninformative dimensions sloppy, i.e., sensitive to perturbations. This constitutes important evidence for earlier theoretical proposals of dimension specific computation since the circuit is built to selectively stabilize the computationally significant dimensions. Finally, we show that this robustness can be achieved by a modular organization of circuitry, whereby modules whose dynamics normally evolve independently can correct each other’s dynamics when an individual module is perturbed, a common design feature in robust systems engineering.

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"This talk explores the possibility that horizontal intra-cortical connections contribute to the dynamic emergence of facilitation and predictions in the primary visual cortex (V1) of cat and non-human primates (NHP)). Contextual long-range interactions, studied at the spiking level, are generally thought to depend on cortico-cortical feedback (Li et al., 2006; Gilbert and Li, 2013) and attention (Lamme & Roelfsema 2000). In contrast, the contribution of intra-V1 mechanisms such as recurrent amplification and lateral propagation (review in Frégnac, 2002 and Frégnac and Bathellier, 2015) is less known.

Experimental work in my lab (UNIC) has been focusing on the dynamic processes based on lateral propagation in V1, through which spatio-temporal inferences (continuous movement or apparent motion sequences) may be generated and facilitate predictive responses along a trajectory (""filling-in""). The stimulation paradigms that we have designed interleave a variety of apparent or continuous animations of local oriented stimuli along trajectories, forming predictable global patterns according to their local to global configuration, and their specific spatial and temporal properties. We have measured the cortical dynamics evoked at two scales of neuronal integration, from micro- (intracellular, SUA) to meso-scopic levels (dense laminar electrode (MEA) and voltage sensitive dye imaging (VSDI)) in the anesthetized cat.

The picture drawn from our intracellular observations is that synaptic activity in cat V1 reveals a built-in bias in the structural organization in the absence of attention-related feedback from higher cortical areas (Gerard-Mercier et al, 2016). This neural process could be related to perceptual biases expressed in NHPs and humans. Taken together with findings obtained in collaboration with the group of Frederic Chavane (INT, Marseille), and based on LFP recordings (Benvenuti et al, submitted), our results suggest, surprisingly, that distinct neural mechanisms - implicating horizontal connectivity - may operate along orthogonal configurations of orientation and direction features and activate differently V1 receptive fields (RF): on one side, surround facilitatory modulation along the orientation preference axis; on the other, anticipatory responses for direction perpendicular to orientation, i.e. along the RF width axis.

Each set of data (still in progress) points to two specific roles of horizontal propagation in V1, with possibly different spatial anisotropy profiles, different spatial scales and different speed selectivities. The first one concerns collinear-biased propagation of iso-orientation preference at high speed (0.1-0.3 m/s; 100°/sec (monkey) -250°/sec (cat)) and fits the general concept of the ""perceptual"" association field” (Field et al, 1993; Li et al, 2006; Gerard-Mercier et al, 2016). The second one concerns isotropic horizontal propagation (10-30°/sec (cat and monkey)) and the directional build-up of anticipatory activity facilitating integration of a moving object along a trajectory (Benevenuti et al, submitted). This propagation process could operate at lower speed than the orientation selective component, and most likely imply a cascade of shorter-range horizontal interactions triggered by a sequence of feedforward inputs. Its synaptic correlates are still unknown.

At a more conceptual level, our working hypothesis posits that horizontal connectivity participates to the propagation of a network-based belief, resulting in some kind of ""prediction"" (filling-in) or ""anticipatory"" build-up process travelling through the V1 network. This view may be compared - and why not opposed - to the classical ""predictive coding"" schema (Rao and Ballard, 1999) where what is transmitted laterally or through feedback onto V1 is the error signal itself (error from the expectation generated in higher cortical areas) rather than the prediction inferred from the global perceptual information. When the contrast is high, the lateral broadcast of the peripheral context leads to a suppression of redundancy of activity in V1 (Martin and von der Heydt, 2015). In contrast when the feedforward signal is weak (low contrast or stimulus absence in ""illusory contour"") the contextual information boosts the gain of feedforward-related activity (Fregnac et al, 1996). Future project development focuses on the possible dependency of the balance between horizontal connectivity and feedback from higher cortical areas on species-specific V1 architecture features and cognitive behavior.

This work, in its initial phase, has been supported by the ramp-up phase of the Human Brain Project (HBP-SP3), and the Marie-Curie Fellowship program. It is currently funded by the CNRS and the French Agence Nationale de la Recherche (ANR: Horizontal-V1).

References :

Benvenuti, G., Chemla, S., Boonman, A., Masson, GS and Chavane F (submitted). Anticipatory responses along motion trajectories in awake monkey V1.
Chavane, F., Sharon, D., Jancke, D., Marre, O., Frégnac, Y., & Grinvald, A. (2011). Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity. Frontiers in Systems Neuroscience, 5(4): 1-26.
Field, D.J., Hayes, A., and Hess, R.F. (1993). Contour integration by the human visual system: evidence for a local “association field.” Vision Research 33, 173–193.
Frégnac, Y. (2012). Reading out the synaptic echoes of low level perception in V1. Lecture Notes in Computer Science. 7583: 486-495
Frégnac, Y. and Bathellier, B. (2015). Cortical correlates of low-level perception : from neural circuits to percepts. Neuron. 88(1): 110-126.Fregnac et al 1996
Frégnac, Y., Bringuier, V. & Chavane, F. (1996) Synaptic integration fields and associative plasticity of visual cortical cells in vivo. Journal of Physiology (Paris) 90:367–372
Gerard-Mercier, F., Pananceau, M., Carelli, P., Troncoso, X. and Frégnac, Y. (2016). Synaptic correlates of low-level perception in V1. The Journal of Neuroscience. 36(14) : 3925-3942.
Gilbert, C. D., & Li, W. (2013). Top-down influences on visual processing. Nature Reviews Neuroscience, 14(5), 350–363. Lamme and Roeflsema
Lamme, V. A., & Roelfsema, P. R. (2000). The distinct modes of vision offered by feedforward and recurrent processing. Trends in Neurosciences, 23(11), 571–579.
Li, W., Piëch, V. & Gilbert, C.D. (2006). Contour saliency in primary visual cortex. Neuron 50:951–962.
Martin, A.B. & von der Heydt, R. (2015). Spike Synchrony Reveals Emergence of Proto-Objects in Visual Cortex. The Journal of  Neuroscience 35: 6860-6870.
Muller, L., Reynaud, A., Chavane, F., & Destexhe, A. (2014). The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave. Nature Communications, 5(3675).
Rao, R.P. and Ballard, D.H. (1999). Predictive coding in the visual cortex : a functional interpretation of some extra-classical receptive-field effects. Nature Neuroscience 2(1): 79-87."

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