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Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks.

ABSTRACT: Pattern separation is a fundamental function of the brain. The divergent feedforward networks thought to underlie this computation are widespread, yet exhibit remarkably similar sparse synaptic connectivity. Marr-Albus theory postulates that such networks separate overlapping activity patterns by mapping them onto larger numbers of sparsely active neurons. But spatial correlations in synaptic input and those introduced by network connectivity are likely to compromise performance. To investigate the structural and functional determinants of pattern separation we built models of the cerebellar input layer with spatially correlated input patterns, and systematically varied their synaptic connectivity. Performance was quantified by the learning speed of a classifier trained on either the input or output patterns. Our results show that sparse synaptic connectivity is essential for separating spatially correlated input patterns over a wide range of network activity, and that expansion and correlations, rather than sparse activity, are the major determinants of pattern separation.

SUBMITTER: Cayco-Gajic NA

PROVIDER: S-EPMC5653655 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks.

Cayco-Gajic N Alex NA Clopath Claudia C Silver R Angus RA

Nature communications 20171024 1

Pattern separation is a fundamental function of the brain. The divergent feedforward networks thought to underlie this computation are widespread, yet exhibit remarkably similar sparse synaptic connectivity. Marr-Albus theory postulates that such networks separate overlapping activity patterns by mapping them onto larger numbers of sparsely active neurons. But spatial correlations in synaptic input and those introduced by network connectivity are likely to compromise performance. To investigate ...[more]

PMID: 29061964

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Project description:The communication of neurons is primarily maintained by synapses, which play a crucial role in the functioning of the nervous system. Therefore, synaptic failure may critically impair information processing in the brain and may underlie many neurodegenerative diseases. A number of studies have suggested that synaptic failure may preferentially target neurons with high connectivity (i.e., network hubs). As a result, the activity of these highly connected neurons can be significantly affected. It has been speculated that anesthetics regulate conscious state by affecting synaptic transmission at these network hubs and subsequently reducing overall coherence in the network activity. In addition, hubs in cortical networks are shown to be more vulnerable to amyloid deposition because of their higher activity within the network, causing decrease in coherence patterns and eventually Alzheimer's disease (AD). Here, we investigate how synaptic failure can affect spatio-temporal dynamics of scale free networks, having a power law scaling of number of connections per neuron - a relatively few neurons (hubs) with a lot of emanating or incoming connections and many cells with low connectivity. We studied two types of synaptic failure: activity-independent and targeted, activity-dependent synaptic failure. We defined scale-free network structures based on the dominating direction of the connections at the hub neurons: incoming and outgoing. We found that the two structures have significantly different dynamical properties. We show that synaptic failure may not only lead to the loss of coherence but unintuitively also can facilitate its emergence. We show that this is because activity-dependent synaptic failure homogenizes the activity levels in the network creating a dynamical substrate for the observed coherence increase. Obtained results may lead to better understanding of changes in large-scale pattern formation during progression of neuro-degenerative diseases targeting synaptic transmission.

Project description:BackgroundFemales are more likely to present with anxiety disorders such as post-traumatic stress disorder (PTSD) compared to males, which are associated with disrupted hippocampal integrity. Sex differences in the structure and function of hippocampus exist. Here, we examined sex differences in contextual pattern separation, functional connectivity, and activation of new neurons during fear memory.MethodsTwo-month-old male and female Sprague-Dawley rats were injected with the DNA synthesis markers, iododeoxyuridine (IdU) and chlorodeoxyuridine (CldU) 3 weeks and 4 weeks before perfusion, respectively. One week after CldU injection, the rats underwent a context discrimination task in which rats were placed in context A (shock) and context A' (no shock) every day for 12 days. On the test day, rats were placed in the shock context (context A) to measure fear memory and expression of zif268, an immediate early gene across 16 different limbic and reward regions. Repeated-measures or factorial analysis of variance was conducted on our variables of interest. Pearson product-moment calculations and principal component analyses on zif268 expression across regions were also performed.ResultsWe found that females, but not males, showed contextual discrimination during the last days of training. On the test day, both sexes displayed similar levels of freezing, indicating equivalent fear memory for context A. Despite similar fear memory, males showed more positive correlations of zif268 activation between the limbic regions and the striatum, whereas females showed more negative correlations among these regions. Females showed greater activation of the frontal cortex, dorsal CA1, and 3-week-old adult-born dentate granular cells compared to males.ConclusionsThese results highlight the importance of studying sex differences in fear memory and the contribution of adult neurogenesis to the neuronal network and may contribute to differences in susceptibility to fear-related disorders such as post-traumatic stress disorder. Highlights Female rats, but not male rats, show faster discrimination during a contextual pattern separation task. Three-week-old adult-born neurons are more active in response to fear memory in females compared to males. Females had greater neural activation compared to males in the frontal cortex and dorsal CA1 region of the hippocampus in response to fear memory. Males and females show distinct patterns in functional connectivity for fear memory across limbic regions. Males have many positive correlations between activated new neurons of different ages between the dorsal and ventral hippocampus, while females show more correlations between activated new neurons and other limbic regions.

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Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks.

Publications

Sparse synaptic connectivity is required for decorrelation and pattern separation in feedforward networks.

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