The systemic effects of the enriched environment on the conditioned fear reaction

Abstract

In this review, a hypothesis is proposed to explain the beneficial effect of an enriched environment (EE) on the conditioned fear reaction (CFR) from the perspective of a functional system of behavioral control. According to the hypothesis, the EE affects all behavioral act components, including the processing of sensory information, memory, motivational and reinforcing systems, and motor activities, which weakens the CFR. Animals raised in the EE have effects that are comparable to those of context (CTX) and CS pre-exposures at latent inhibition. An abundance of stimuli in the EE and constant contact with them provide the formation of CS-noUS and CTX-noUS connections that later, during CFR learning, slow down and diminish fear. The EE also contributes to faster processing of information and habituation to it. As a result, many stimuli in the context lose their significance, and subjects simply ignore them. And finally, the EE affects the motivational and reinforcing brain mechanisms, induces an impairment of search activity, and worsens memory consolidation, which leads to a reduction of CFR.

Keywords: conditioned fear reaction; context; enriched environment; information processing; memory; motivation; reinforcement.

FIGURE 1

The functional system of behavioral control–how it works and how the EE has a beneficial impact on its work in the case of fear conditioning. The functional system of behavioral control represents an integrated framework of key components, including memory, sensory information, motivation, actions, and reinforcement. It consists of two main parts: sensory-motivational (orange color) and motor-reinforcing (green color) circuits. They are linked within the memory apparatus by stimulus-motor connections (S-R connections or engrams), which are organized on the complementary (“lock and key”) principle. Formation of a new stimulus-motor connection requires, on the one hand, activation of the motivational structures by a proper real stimulus via a forward conditional connection, and, on the other, formation of a trace or sensory engram in the central memory-related structures corresponding to this stimulus. It is also possible to activate the sensory-motivational subsystem from the motivational input. In this case, the motivational excitation, on the one hand, will activate the sensory engrams of different stimuli, and on the other hand, through activation of the backward conditional connection, induce the subject’s search for those stimuli that correspond to sensory engrams that led in the past to receiving reinforcement. Thus, in the sensory-motivational subsystem forming the first closed neuro-functional circuit, events develop in the following scenario: the inflow of current sensory information; trigger, with its assistance, the motivational mechanisms of the brain; actualization through signal and motivational excitations of sensory engrams of memory; comparison and evaluation of matching (or not matching) of the stored engrams with proper incoming environmental stimuli. When the sensory engrams coincide with the acting stimuli, the complementary motor engrams are actualized and excitation is transferred to the motor-reinforcement subsystem. The sensory and motor engrams form their own internal subsystem of connections in the memory apparatus, which overall are organized as a second neuro-functional circuit. The motor-reinforcement subsystem includes the executive mechanisms of actions, the mechanisms of reinforcement (emotions), and motor engrams (traces of motor experience) in the motor part of memory (shown by the green color). Overall, these functional blocks form a third neuro-functional circuit, which is closed by feedback connections from the reinforcing structures to the memory engrams. If the result of action has valuable or adaptational significance for the organism, the corresponding stimulus-motor engrams are strengthened and reinforced (Grigoryan, 1990, 2006; Grigoryan and Gulyaeva, 2017). The blue arrows show the influence of the enriched environment on manifestations of the conditioned fear response. As is seen from the figure, the EE affects every link of the functional system. At the level of the memory structures, the EE weakens the formation of conditioned (S-S) connections between the signal and the unconditional stimulus (CS-US) and between the context and the unconditional stimulus (CTX-US). This happens due to the fast adaptation of animals being in the EE to the surrounding world, which promotes an impaired incorporation of sensory stimuli into the contextual fear memory (formation of the sensory engrams). On the other hand, the quick loss of interest in these stimuli in the EE animals weakens the motivational state and, in addition to the weak impact of natural stimuli, further impairs the formation of sensory engrams. The weakening of the S-S associations under the effects of EE during fear conditioning reminds the effects of latent inhibition. Thus, the EE impairs the function of the sensory-motivational circuit and formation of the sensory engrams in the memory structures. But apart from the problems in the sensory part of the memory, the EE affects locomotor activity and reinforcement function, bringing problems with the formation of motor engrams and consolidation of fear memory. Thus, again, this all acts against the conditioned fear response, and promotes the beneficial effects of the EE. More full explanations, supported by the literature data are given in the text.