The neuroscience of mammalian associative learning.

Department of Psychology and Brain Research Institute, University of California-Los Angeles, Los Angeles, CA 90095-1563, USA.
Annual Review of Psychology (Impact Factor: 20.53). 02/2005; 56:207-34. DOI: 10.1146/annurev.psych.56.091103.070213
Source: PubMed

ABSTRACT Mammalian associative learning is organized into separate anatomically defined functional systems. We illustrate the organization of two of these systems, Pavlovian fear conditioning and Pavlovian eyeblink conditioning, by describing studies using mutant mice, brain stimulation and recording, brain lesions and direct pharmacological manipulations of specific brain regions. The amygdala serves as the neuroanatomical hub of the former, whereas the cerebellum is the hub of the latter. Pathways that carry information about signals for biologically important events arrive at these hubs by circuitry that depends on stimulus modality and complexity. Within the amygdala and cerebellum, neural plasticity occurs because of convergence of these stimuli and the biologically important information they predict. This neural plasticity is the physical basis of associative memory formation, and although the intracellular mechanisms of plasticity within these structures share some similarities, they differ significantly. The last Annual Review of Psychology article to specifically tackle the question of mammalian associative learning ( Lavond et al. 1993 ) persuasively argued that identifiable "essential" circuits encode memories formed during associative learning. The next dozen years saw breathtaking progress not only in detailing those essential circuits but also in identifying the essential processes occurring at the synapses (e.g., Bi & Poo 2001, Martinez & Derrick 1996 ) and within the neurons (e.g., Malinow & Malenka 2002, Murthy & De Camilli 2003 ) that make up those circuits. In this chapter, we describe the orientation that the neuroscience of learning has taken and review some of the progress made within that orientation.

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Available from: Michael Fanselow, Jul 08, 2015
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    • "It offers an analogue model to study processes that play a role in the pathogenesis and treatment of anxiety disorders (Mineka & Zinbarg, 2006). Over the past decennia, fear conditioning research in animals and humans has unraveled key processes involved in the formation, consolidation and expression of associative fear memories (e.g., see Craske, Hermans, & Vansteenwegen, 2006; Fanselow & Poulos, 2005; LeDoux, 2000), which are supposed to lie at the root of anxiety disorders. "
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    ABSTRACT: We argue that the stimuli used in traditional fear conditioning paradigms are too simple to model the learning and unlearning of complex fear memories. We therefore developed and tested an adapted fear conditioning paradigm, specifically designed for the study of complex associative memories. Second, we explored whether manipulating the meaning and complexity of the CS-UCS association strengthened the learned fear association.Methods In a two-day differential fear conditioning study, participants were randomly assigned to two experimental conditions. All participants were subjected to the same CSs (i.e., pictures) and UCS (i.e., 3 sec film clip) during fear conditioning. However, in one of the conditions (negative-relevant context), the reinforced CS and UCS were meaningfully connected to each other by a 12 min aversive film clip presented prior to fear acquisition. Participants in the other condition (neutral context) were not able to make such meaningful connection between these stimuli, as they viewed a neutral film clip.ResultsFear learning and unlearning were observed on fear-potentiated startle data and distress ratings within the adapted paradigm. Moreover, several group differences on these measures indicated increased UCS valence and enhanced associative memory strength in the negative-relevant context condition compared to the neutral context condition.LimitationsDue to technical equipment failure, skin conductance data could not be interpreted.Conclusions The fear conditioning paradigm as presented in the negative-relevant context condition holds considerable promise for the study of complex associative fear memories and therapeutic interventions for such memories.
    Journal of Behavior Therapy and Experimental Psychiatry 11/2014; DOI:10.1016/j.jbtep.2014.11.007 · 2.23 Impact Factor
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    • "Within the amygdala, an abundance of research indicates that long-term potentiation (LTP) is a mechanism for fear conditioning (Blair et al., 2001; Davis and Whalen, 2001; Fanselow and Poulos, 2005; Goosens and Maren, 2002; LeDoux, 2000; Maren, 2001; 1999; Maren and Quirk, 2004; Sigurdsson et al., 2007). Amygdaloid LTP was first described in extracellular field recordings in vivo (Clugnet and LeDoux, 1990; Racine et al., 1983) and subsequently confirmed by intracellular recordings of synaptic currents in lateral nucleus (LA) neurons in vitro (Chapman and Bellavance, 1992; Chapman et al., 1990). "
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    ABSTRACT: Considerable research indicates that long-term synaptic plasticity in the amygdala underlies the acquisition of emotional memories, including those learned during Pavlovian fear conditioning. Much less is known about the synaptic mechanisms involved in other forms of associative learning, including extinction, that update fear memories. Extinction learning might reverse conditioning-related changes (e.g., depotentiation) or induce plasticity at inhibitory synapses (e.g., long-term potentiation) to suppress conditioned fear responses. Either mechanism must account for fear recovery phenomena after extinction, as well as savings of extinction after fear recovery.
    Brain Research 10/2014; DOI:10.1016/j.brainres.2014.10.010 · 2.83 Impact Factor
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    • "In a typical experiment, rats are trained to shuttle across a divided chamber during auditory CS presentation, causing termination of the CS and omission of the footshock US (Choi et al., 2010; Ledoux, 2014). Importantly, while AA requires Pavlovian learning to encode threat, the transition to successful instrumental avoidance requires active suppression of freezing (Lázaro-Muñoz et al., 2010; Moscarello and Ledoux, 2013), an innate defensive response to a Pavlovian CS (Blanchard and Blanchard, 1969; Fanselow and Poulos, 2005). Animals do not uniformly learn signaled AA. "
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    ABSTRACT: Individuals exposed to traumatic stressors follow divergent patterns including resilience and chronic stress. However, researchers utilizing animal models that examine learned or instrumental threat responses thought to have translational relevance for Posttraumatic Stress Disorder (PTSD) and resilience typically use central tendency statistics that assume population homogeneity. This approach potentially overlooks fundamental differences that can explain human diversity in response to traumatic stressors. The current study tests this assumption by identifying and replicating common heterogeneous patterns of response to signaled active avoidance (AA) training. In this paradigm, rats are trained to prevent an aversive outcome (shock) by performing a learned instrumental behavior (shuttling between chambers) during the presentation of a conditioned threat cue (tone). We test the hypothesis that heterogeneous trajectories of threat avoidance provide more accurate model fit compared to a single mean trajectory in two separate studies. Study 1 conducted 3 days of signaled AA training (n = 81 animals) and study 2 conducted 5 days of training (n = 186 animals). We found that four trajectories in both samples provided the strongest model fit. Identified populations included animals that acquired and retained avoidance behavior on the first day (Rapid Avoiders: 22 and 25%); those who never successfully acquired avoidance (Non-Avoiders; 20 and 16%); a modal class who acquired avoidance over 3 days (Modal Avoiders; 37 and 50%); and a population who demonstrated a slow pattern of avoidance, failed to fully acquire avoidance in study 1 and did acquire avoidance on days 4 and 5 in study 2 (Slow Avoiders; 22.0 and 9%). With the exception of the Slow Avoiders in Study 1, populations that acquired demonstrated rapid step-like increases leading to asymptotic levels of avoidance. These findings indicate that avoidance responses are heterogeneous in a way that may be informative for understanding both resilience and PTSD as well as the nature of instrumental behavior acquisition. Characterizing heterogeneous populations based on their response to threat cues would increase the accuracy and translatability of such models and potentially lead to new discoveries that explain diversity in instrumental defensive responses.
    Frontiers in Systems Neuroscience 09/2014; 8. DOI:10.3389/fnsys.2014.00179