Integration of exteroceptive and interoceptive information within the hippocampus: a computational study

International audienceCitation: Kassab R and Alexandre F (2015) Integration of exteroceptive and interoceptive information within the hippocampus: a computational study. Front. Syst. Neurosci. 9:87. Many episodic memory studies have critically implicated the hippocampus in the rapid binding of sensory information from the perception of the external environment, reported by exteroception. Other structures in the medial temporal lobe, especially the amygdala, have been more specifically linked with emotional dimension of episodic memories, reported by interoception. The hippocampal projection to the amygdala is proposed as a substrate important for the formation of extero-interoceptive associations, allowing adaptive behaviors based on past experiences. Recently growing evidence suggests that hippocampal activity observed in a wide range of behavioral tasks could reflect associations between exteroceptive patterns and their emotional valences. The hippocampal computational models, therefore, need to be updated to elaborate better interpretation of hippocampal-dependent behaviors. In earlier models, interoceptive features, if not neglected, are bound together with other exteroceptive features through autoassociative learning mechanisms. This way of binding integrates both kinds of features at the same level, which is not always suitable for example in the case of pattern completion. Based on the anatomical and functional heterogeneity along the septotemporal and transverse axes of the hippocampus, we suggest instead that distinct hippocampal subregions may be engaged in the representation of these different types of information, each stored apart in autoassociative memories but linked together in a heteroassociative way. The model is developed within the hard constraint of rapid, even single trial, learning of episodic memories. The performance of the model is assessed quantitatively and its resistance to interference is demonstrated through a series of numerical experiments. An experiment of reversal learning in patients with amnesic cognitive impairment is also reproduced

Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine

ABSTRACT: In order to understand how the molecular or cellular defects that underlie a disease of the nervous system lead to the observ-able symptoms, it is necessary to develop a large-scale neural model. Such a model must specify how specific molecular processes contribute to neuronal function, how neurons contribute to network function, and how networks interact to produce behavior. This is a challenging undertaking, but some limited progress has been made in understanding the memory functions of the hippocampus with this degree of detail. There is increas-ing evidence that the hippocampus has a special role in the learning of sequences and the linkage of specific memories to context. In the first part of this paper, we review a model (the SOCRATIC model) that describes how the dentate and CA3 hippocampal regions could store and recall memory sequences in context. A major line of evidence for sequence recall is the “phase precession ” of hippocampal place cells. In the second part of the paper, we review the evidence for theta-gamma phase coding

Improving Associative Memory in a Network of Spiking Neurons

In this thesis we use computational neural network models to examine the dynamics and functionality of the CA3 region of the mammalian hippocampus. The emphasis of the project is to investigate how the dynamic control structures provided by inhibitory circuitry and cellular modification may effect the CA3 region during the recall of previously stored information. The CA3 region is commonly thought to work as a recurrent auto-associative neural network due to the neurophysiological characteristics found, such as, recurrent collaterals, strong and sparse synapses from external inputs and plasticity between coactive cells. Associative memory models have been developed using various configurations of mathematical artificial neural networks which were first developed over 40 years ago. Within these models we can store information via changes in the strength of connections between simplified model neurons (two-state). These memories can be recalled when a cue (noisy or partial) is instantiated upon the net. The type of information they can store is quite limited due to restrictions caused by the simplicity of the hard-limiting nodes which are commonly associated with a binary activation threshold. We build a much more biologically plausible model with complex spiking cell models and with realistic synaptic properties between cells. This model is based upon some of the many details we now know of the neuronal circuitry of the CA3 region. We implemented the model in computer software using Neuron and Matlab and tested it by running simulations of storage and recall in the network. By building this model we gain new insights into how different types of neurons, and the complex circuits they form, actually work. The mammalian brain consists of complex resistive-capacative electrical circuitry which is formed by the interconnection of large numbers of neurons. A principal cell type is the pyramidal cell within the cortex, which is the main information processor in our neural networks. Pyramidal cells are surrounded by diverse populations of interneurons which have proportionally smaller numbers compared to the pyramidal cells and these form connections with pyramidal cells and other inhibitory cells. By building detailed computational models of recurrent neural circuitry we explore how these microcircuits of interneurons control the flow of information through pyramidal cells and regulate the efficacy of the network. We also explore the effect of cellular modification due to neuronal activity and the effect of incorporating spatially dependent connectivity on the network during recall of previously stored information. In particular we implement a spiking neural network proposed by Sommer and Wennekers (2001). We consider methods for improving associative memory recall using methods inspired by the work by Graham and Willshaw (1995) where they apply mathematical transforms to an artificial neural network to improve the recall quality within the network. The networks tested contain either 100 or 1000 pyramidal cells with 10% connectivity applied and a partial cue instantiated, and with a global pseudo-inhibition.We investigate three methods. Firstly, applying localised disynaptic inhibition which will proportionalise the excitatory post synaptic potentials and provide a fast acting reversal potential which should help to reduce the variability in signal propagation between cells and provide further inhibition to help synchronise the network activity. Secondly, implementing a persistent sodium channel to the cell body which will act to non-linearise the activation threshold where after a given membrane potential the amplitude of the excitatory postsynaptic potential (EPSP) is boosted to push cells which receive slightly more excitation (most likely high units) over the firing threshold. Finally, implementing spatial characteristics of the dendritic tree will allow a greater probability of a modified synapse existing after 10% random connectivity has been applied throughout the network. We apply spatial characteristics by scaling the conductance weights of excitatory synapses which simulate the loss in potential in synapses found in the outer dendritic regions due to increased resistance. To further increase the biological plausibility of the network we remove the pseudo-inhibition and apply realistic basket cell models with differing configurations for a global inhibitory circuit. The networks are configured with; 1 single basket cell providing feedback inhibition, 10% basket cells providing feedback inhibition where 10 pyramidal cells connect to each basket cell and finally, 100% basket cells providing feedback inhibition. These networks are compared and contrasted for efficacy on recall quality and the effect on the network behaviour. We have found promising results from applying biologically plausible recall strategies and network configurations which suggests the role of inhibition and cellular dynamics are pivotal in learning and memory

A Heteroassociative Learning Model Robust to Interference

Best Paper AwardInternational audienceNeuronal models of associative memories are recurrent networks able to learn quickly patterns as stable states of the network. Their main acknowledged weakness is related to catastrophic interference when too many or too close examples are stored. Based on biological data we have recently proposed a model resistant to some kinds of interferences related to heteroassociative learning. In this paper we report numerical experiments that highlight this robustness and demonstrate very good performances of memorization. We also discuss convergence of interests for such an adaptive mechanism for biological modeling and information processing in the domain of machine learning

A Modular Network Architecture Resolving Memory Interference through Inhibition

International audienceIn real learning paradigms like pavlovian conditioning, several modes of learning are associated, including generalization from cues and integration of specific cases in context. Associative memories have been shown to be interesting neuronal models to learn quickly specific cases but they are hardly used in realistic applications because of their limited storage capacities resulting in interferences when too many examples are considered. Inspired by biological considerations, we propose a modular model of associative memory including mechanisms to manipulate properly multimodal inputs and to detect and manage interferences. This paper reports experiments that demonstrate the good behavior of the model in a wide series of simulations and discusses its impact both in machine learning and in biological modeling