A neural model of normal and abnormal learning and memory consolidation: adaptively timed conditioning, hippocampus, amnesia, neurotrophins, and consciousness

Daniel J Franklin,Stephen Grossberg

doi:10.3758/s13415-016-0463-y

Abstract

How do the hippocampus and amygdala interact with thalamocortical systems to regulate cognitive and cognitive-emotional learning? Why do lesions of thalamus, amygdala, hippocampus, and cortex have differential effects depending on the phase of learning when they occur? In particular, why is the hippocampus typically needed for trace conditioning, but not delay conditioning, and what do the exceptions reveal? Why do amygdala lesions made before or immediately after training decelerate conditioning while those made later do not? Why do thalamic or sensory cortical lesions degrade trace conditioning more than delay conditioning? Why do hippocampal lesions during trace conditioning experiments degrade recent but not temporally remote learning? Why do orbitofrontal cortical lesions degrade temporally remote but not recent or post-lesion learning? How is temporally graded amnesia caused by ablation of prefrontal cortex after memory consolidation? How are attention and consciousness linked during conditioning? How do neurotrophins, notably brain-derived neurotrophic factor (BDNF), influence memory formation and consolidation? Is there a common output path for learned performance? A neural model proposes a unified answer to these questions that overcome problems of alternative memory models.

Highlights

Trace conditioning involves a temporal gap between conditioned stimulus (CS) offset and unconditioned stimulus (US) onset such that a CS-activated memory trace is required during the inter-stimulus interval (ISI) in order to establish an adaptively timed association between CS and US that leads to a successful conditioned response (CR) (Pavlov, 1927)
We show below that this amygdala-based process is effective during delay conditioning, where the CS and US overlap in time, but not during trace conditioning, where the CS terminates before the US begins, at least not without the benefit of the adaptively timed learning mechanisms that are described
There is adaptively-timed learning of motor responses via the cerebellum (Figure 16), but this is not simulated in the current study

Summary

Introduction

The roles and interactions of amygdala, hippocampus, thalamus, and neocortex in cognitive and cognitive-emotional learning, memory, and consciousness have been extensively investigated through experimental and clinical studies (Berger & Thompson, 1978; Clark, Manns, & Squire, 2001; Frankland & Bontempi, 2005; Kim, Clark, & Thompson, 1995; Lee & Kim, 2004; Mauk & Thompson 1987; Moustafa et al, 2013; Port, Romano, Steinmetz, Mikhail, & Patterson, 1986; Powell & Churchwell, 2002; Smith, 1968; Takehara, Kawahara, & Krino, 2003). The model clarifies why the hippocampus is needed for trace conditioning, but not delay conditioning (Büchel et al, 1999; Frankland & Bontempi, 2005; Green & Woodruff-Pak, 2000; Kaneko & Thompson, 1997; Kim, Clark, & Thompson, 1995; Port et al, 1986; Takehara, Kawahara, & Krino, 2003); why thalamic lesions retard the acquisition of trace conditioning (Powell & Churchwell, 2002), but have less of a statistically significant effect on delay conditioning (Buchanan & Thompson, 1990); why early but not late amygdala lesions degrade both delay conditioning (Lee & Kim, 2004) and trace conditioning (Büchel et al, 1999); why hippocampal lesions degrade recent but not temporally remote trace conditioning (Kim et al, 1995; Takehara et al, 2003); why in delay conditioning, such lesions typically have no negative impact on CR performance but this finding may vary with experimental preparation and CR success criteria (Berger, 1984; Chen et al, 1995; Lee & Kim, 2004; Port, 1985; Shors, 1992; Moustafa, et al, 2013); why cortical lesions degrade temporally remote but not recent trace conditioning, but have no impact on the acquisition of delay conditioning (Frankland & Bontempi, 2005; Kronforst-Collins & Disterhoft, 1998; McLaughlin et al, 2002; Takehara et al, 2003; see Oakley & Steele Russell, 1972; Yeo, Hardiman, Moore, & Steele Russell,.1984); how temporally-graded amnesia may be caused by ablation of the medial prefrontal cortex after memory consolidation (Simon, Knuckley, Churchwell, & Powell, 2005; Takehara et al, 2003; Weible, McEchron, & Disterhoft, 2000); how attention and consciousness are linked during delay and trace conditioning (Clark, Manns, & Squire, 2002; Clark & Squire, 1998, 2010); and how neurotrophins, notably brain-derived neurotrophic factor (BDNF), influence memory formation and consolidation (Kokaia et al, 1993, Tyler et al, 2002)

Methods

Results

Conclusion