Abstract
This work studies the evolution of cortical networks during the transition from escape strategy to avoidance strategy in auditory discrimination learning in Mongolian gerbils trained by the well-established two-way active avoidance learning paradigm. The animals were implanted with electrode arrays centered on the surface of the primary auditory cortex and electrocorticogram (ECoG) recordings were made during performance of an auditory Go/NoGo discrimination task. Our experiments confirm previous results on a sudden behavioral change from the initial naïve state to an avoidance strategy as learning progresses. We employed two causality metrics using Granger Causality (GC) and New Causality (NC) to quantify changes in the causality flow between ECoG channels as the animals switched to avoidance strategy. We found that the number of channel pairs with inverse causal interaction significantly increased after the animal acquired successful discrimination, which indicates structural changes in the cortical networks as a result of learning. A suitable graph-theoretical model is developed to interpret the findings in terms of cortical networks evolving during cognitive state transitions. Structural changes lead to changes in the dynamics of neural populations, which are described as phase transitions in the network graph model with small-world connections. Overall, our findings underscore the importance of functional reorganization in sensory cortical areas as a possible neural contributor to behavioral changes.
Highlights
There is a growing body of literature on the neural basis of learning and memory formation over various sensory modalities in humans and animals (Goldstone, 1998; Seger and Miller, 2010; Chapuis and Wilson, 2012; Aizenberg and Geffen, 2013)
We investigated how pairwise causal interactions between channels of the surface electrode array were affected by the progression of the learning
We studied inverse causality flows for conditioned stimulus (CS)+ and CS− stimuli, using the wellestablished Granger Causality (GC) and the recently introduced New Causality (NC)
Summary
There is a growing body of literature on the neural basis of learning and memory formation over various sensory modalities in humans and animals (Goldstone, 1998; Seger and Miller, 2010; Chapuis and Wilson, 2012; Aizenberg and Geffen, 2013). State Transitions in Auditory Discriminatory Learning including primary and higher-order auditory cortex (Eggermont et al, 1983; Weinberger et al, 1984; Ohl and Scheich, 1996; Villa et al, 1998, 1999a; Fritz et al, 2003; Weinberger, 2004, 2007; Plakke et al, 2013; Grosso et al, 2015, 2017; Cambiaghi et al, 2016; Concina et al, 2018), corpus striatum (Znamenskiy and Zador, 2013), and prefrontal cortex (Romanski et al, 1999; Funamizu et al, 2013; Concina et al, 2018) In such neural structures, the responses of single neurons and population of neurons to relevant spectral, temporal, or spectrotemporal features of stimuli undergo changes when these features attain behavioral or cognitive relevance during learning or specific task scenarios (Villa et al, 1999b; Machens et al, 2004; Ohl and Scheich, 2005; Bar-Yosef and Nelken, 2007; Schreiner and Winer, 2007; Rabinowitz et al, 2013; Meyer et al, 2014; Weinberger, 2015). The behavioral process and its underlying mechanisms are akin to Pavlovian conditioning in which a conditioned stimulus (CS) is learned to have predictive power for the occurrence of an unconditioned stimulus (US)
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