Nonassociative Processes Research Articles

The irreconcilability of insight

We are said to experience insight when we suddenly and unexpectedly become aware of the solution to a problem that we previously took ourselves to be unable to solve. In the field of comparative cognition, there is rising interest in the question of whether non-human animals are capable of insightful problem-solving. Putative cases of animals demonstrating insight have generally attracted two types of criticism: first, that insight is being conflated with other cognitive capacities (e.g., causal cognition, or mental trial and error); and, second, that the relevant performances merely reflect associative learning—and on the received understanding of insight within comparative cognition, insight necessarily involves non-associative processes. I argue that even if we grant that some cases of animal insight do withstand these two criticisms, these cases of purported animal insight cannot shed light on the nature of insightful problem-solving in humans. For the phenomenon studied by cognitive psychologists under the heading of insight is fundamentally different from that studied in comparative cognition. In light of this impasse, I argue that the reinterpretation of the extant research on animal insight in terms of other high-level cognitive capacities (means-end reasoning in particular) can improve the prospect of a successful comparative research program.

Conditional and unconditional components of aversively motivated freezing, flight and darting in mice.

Fear conditioning is one of the most frequently used laboratory procedures for modeling learning and memory generally, and anxiety disorders in particular. The conditional response (CR) used in the majority of fear conditioning studies in rodents is freezing. Recently, it has been reported that under certain conditions, running, jumping, or darting replaces freezing as the dominant CR. These findings raise both a critical methodological problem and an important theoretical issue. If only freezing is measured but rodents express their learning with a different response, then significant instances of learning, memory, or fear may be missed. In terms of theory, whatever conditions lead to these different behaviors may be a key to how animals transition between different defensive responses and different emotional states. In mice, we replicated these past results but along with several novel control conditions. Contrary to the prior conclusions, running and darting were primarily a result of nonassociative processes and were actually suppressed by associative learning. Darting and flight were taken to be analogous to nonassociative startle or alpha responses that are potentiated by fear. Additionally, associative processes had some impact on the topography of flight behavior. On the other hand, freezing was the purest reflection of associative learning. We also uncovered a rule that describes when these movements replace freezing: when afraid, freeze until there is a sudden novel change in stimulation, then burst into vigorous flight attempts. This rule may also govern the change from fear to panic.

Effects of pre-exposure and post-exposure of the context in habituation of the retraction response in earthworms (Lumbricidae)

The context specificity of habituation has been demonstrated in earthworms. After the habituation of the retraction response to a light, a recovery of the response was observed when subjects are re-habituated in a different context. Some theories assume that an association between the context and the unconditioned stimulus could underlie this result. A series of experiments were conducted in order to test this issue. We assessed the potential disruptive effects of post-exposure (extinction effect) and pre-exposure of the context (latent inhibition effect) on the establishment of a context-US association. A recovery of response during subsequent rehabituation test was expected. The results of Experiment 1 showed that the extinction was effective, the post-exposure of the context after habituation produced a recovery of the retraction response. This result was replicated in Experiment 2 where the post-exposure condition was compared with a pre-exposure one. However, the pre-exposure to the context did not result in a recovery of the response in the rehabituation test, but also produced a general decrement on the response during the habituation training, that it has been interpreted as decrement in context’s salience. In summary, these results suggest the involvement of associative and nonassociative processes in habituation learning.

Dominant parameter of galvanic vestibular stimulation for the non-associative learning processes.

Electrical stimulus is one of the common stimulating methods, and Galvanic vestibular stimulation (GVS) is the oldest form as an electrical stimulation. Nevertheless, GVS is still considered as a secondary stimulating tool for the medical purposes. Even though some unarguable findings have made using GVS, its use has been limited because of its ambiguity as an input source. For better understanding, many previous studies mainly focused on its functional effects, like the ocular reflexes. However, its fundamental effects on the neural activities are still elusive, such as the dominant influences by different parameters of GVS. Here we compared the effects on the neuronal responses by applying two different parameters, strength and rate, of GVS. To assess the dominance on the neuronal responses to these parameters, we designed three independent stimuli. Those stimuli were multiply applied to obtain the responding slopes based on the mechanism of non-associative learning processes, and the effects on the neurons were calculated as an inner angle between two responding slopes. Out of 23 neurons, 15 (65.2%) units were affected more by the strength with a statistical significance (p= 0.047). The ranges of the inner angles also implied the strength (- 3.354°~2.063°) mainly modulated by the neuronal responses comparing with those by the rate (- 2.001°~1.975°). The dominance of the parameters was closely related with the neuronal sensitivity to stimulation (SE) (p= 0.018), while there were few relations with the neuronal regularity, directional preference (DP), and the physiological response (PR) (p> 0.059). Thus, the neural information related with the dominance was delivered by the irregular neurons, and these types of neurons should be the targets for the stimulation. Graphical abstract.

Dissociable learning processes, associative theory, and testimonial reviews: A comment on Smith and Church (2018).

Smith and Church (Psychonomic Bulletin & Review, 25, 1565-1584 2018) present a "testimonial" review of dissociable learning processes in comparative and cognitive psychology, by which we mean they include only the portion of the available evidence that is consistent with their conclusions. For example, they conclude that learning the information-integration category-learning task with immediate feedback is implicit, but do not consider the evidence that people readily report explicit strategies in this task, nor that this task can be accommodated by accounts that make no distinction between implicit and explicit processes. They also consider some of the neuroscience relating to information-integration category learning, but do not report those aspects that are more consistent with an explicit than an implicit account. They further conclude that delay conditioning in humans is implicit, but do not report evidence that delay conditioning requires awareness; nor do they present the evidence that conditioned taste aversion, which should be explicit under their account, can be implicit. We agree with Smith and Church that it is helpful to have a clear definition of associative theory, but suggest that their definition may be unnecessarily restrictive. We propose an alternative definition of associative theory and briefly describe an experimental procedure that we think may better distinguish between associative and non-associative processes.

Saving the Perruchet effect: A role for the strength of the association in associative learning.

In a partial reinforcement schedule where a cue repeatedly predicts the occurrence of a target in consecutive trials, reaction times to the target tend to decrease in a monotonic fashion, while participants' expectancies for the target decrease at the same time. This dissociation between reaction times and expectancies-the so-called Perruchet effect-challenges the propositional view of learning, which posits that human conditioned responses result from conscious inferences about the relationships between events. However, whether the reaction time pattern reflects the strength of a putative cue-target link, or only non-associative processes, such as motor priming, remains unclear. To address this issue, we implemented the Perruchet procedure in a two-choice reaction time task and compared reaction time patterns in an Experimental condition, in which a tone systematically preceded a visual target, and in a Control condition, in which the onset of the two stimuli were uncoupled. Participants' expectancies regarding the target were recorded separately in an initial block. Reaction times decreased with the succession of identical trials in both conditions, reflecting the impact of motor priming. Importantly, reaction time slopes were steeper in the Experimental than in the Control condition, indicating an additional influence of the associative strength between the two stimuli. Interestingly, slopes were less steep for participants who showed the gambler's fallacy in the initial block. In sum, our results suggest the mutual influences of motor priming, associative strength, and expectancies on performance. They are in line with a dual-process model of learning involving both a propositional reasoning process and an automatic link-formation mechanism.

Task switching in rhesus macaques (Macaca mulatta) and tufted capuchin monkeys (Cebus apella) during computerized categorization tasks.

The present experiments extended to monkeys a previously used abstract categorization procedure (Castro & Wasserman, 2016) where pigeons had categorized arrays of clipart icons based upon two task rules: the number of clipart objects in the array or the variability of objects in the array. Experiment 1 replicated Castro and Wasserman by using capuchin monkeys and rhesus monkeys and reported that monkeys' performances were similar to pigeons' in terms of acquisition, pattern of errors, and the absence of switch costs. Furthermore, monkeys' insensitivity to the added irrelevant information suggested that an associative (rather than rule-based) categorization mechanism was dominant. Experiment 2 was conducted to include categorization cue reversals to determine (a) whether the monkeys would quickly adapt to the reversals and inhibit interference from a prereversal task rule (consistent with a rule-based mechanism) and (b) whether the latency to make a response prior to a correct or incorrect outcome was informative about the presence of a cognitive mechanism. The cue reassignment produced profound and long-lasting performance deficits, and a long reacquisition phase suggested the involvement of associative learning processes; however, monkeys also displayed longer latencies to choose prior to correct responses on challenging trials, suggesting the involvement of nonassociative processes. Together these performances suggest a mix of associative and cognitive-control processes governing monkey categorization judgments. (PsycINFO Database Record

Human latent inhibition and the density of predictive relationships in the context in which the target stimulus occurs.

In two experiments, participants were exposed to a listing of actions performed by a fictitious Mr. X, over three days of his life. For most of his actions an outcome was described, but some were not followed by any outcome. On Day 3, Mr. X performed an action (the target action) that was followed by a novel outcome. For participants in the control condition, the target action that preceded the appearance of this outcome was also novel; for participants in the latent inhibition (LI) condition, Mr. X had performed the target action on repeated occasions during Days 2 and 3, without it producing any outcome. All the participants were tested on their ability to retrieve the action performed by Mr. X prior to the target outcome. In Experiment 1, retrieval of the target action (indicating a less effective target action-outcome association) was poorer in the LI than in the control condition. In Experiment 2, reducing the proportion (the density) of nontarget actions that brought outcomes during initial training was found to reduce the size of the LI effect. These results are predicted by the account of LI put forward previously [Hall, G., & Rodríguez, G. (2010). Associative and nonassociative processes in latent inhibition: An elaboration of the Pearce-Hall model. In R. E. Lubow & I. Weiner (Eds.), Latent inhibition: Data, theories, and applications to schizophrenia (pp. 114-136). Cambridge, England: Cambridge University Press]. A high density of predictive relationships ensures strong activation of the expectancy that some outcome will occur when the target action is first presented; this facilitates the formation of a target action-no-event association during training in the LI condition, thus enhancing the LI effect.

Attitudinal and non-attitudinal components of IAT performance.

The Implicit Association Test (IAT) was designed to measure automatically activated attitudinal associations, free of the influence of processes that affect their expression. Subsequent research has shown that IAT performance also is influenced by non-associative processes, but the extent to which these non-associative processes are content-specific or if they operate similarly regardless of the attitude being measured has largely gone unexamined. In the current research, participants completed pairs of IATs that varied in conceptual overlap: Tests shared a high, moderate, or low degree of overlap in the measured attitudes. The Quad model was applied to estimate the contributions of four processes to IAT performance. Evidence was found for two relatively general, non-attitudinal processes and two relatively attitude-specific processes. Implications are discussed for interpretation of IAT scores, individual differences in IAT scores, and IAT score malleability.

Chronic stress disrupts fear extinction and enhances amygdala and hippocampal Fos expression in an animal model of post-traumatic stress disorder

Chronic stress may impose a vulnerability to develop maladaptive fear-related behaviors after a traumatic event. Whereas previous work found that chronic stress impairs the acquisition and recall of extinguished fear, it is unknown how chronic stress impacts nonassociative fear, such as in the absence of the conditioned stimulus (CS) or in a novel context. Male rats were subjected to chronic stress (STR; wire mesh restraint 6h/d/21d) or undisturbed (CON), then tested on fear acquisition (3 tone-footshock pairings), and two extinction sessions (15 tones/session) within the same context. Then each group was tested (6 tones) in the same context (SAME) or a novel context (NOVEL), and brains were processed for functional activation using Fos immunohistochemistry. Compared to CON, STR showed facilitated fear acquisition, resistance to CS extinction on the first extinction day, and robust recovery of fear responses on the second extinction day. STR also showed robust freezing to the context alone during the first extinction day compared to CON. When tested in the same or a novel context, STR exhibited higher freezing to context than did CON, suggesting that STR-induced fear was independent of context. In support of this, STR showed increased Fos-like expression in the basolateral amygdala and CA1 region of the hippocampus in both the SAME and NOVEL contexts. Increased Fos-like expression was also observed in the central amygdala in STR-NOVEL vs. CON-NOVEL. These data demonstrate that chronic stress enhances fear learning and impairs extinction, and affects nonassociative processes as demonstrated by enhanced fear in a novel context.

Implicit Attitudes Reflect Associative, Non‐associative, and Non‐attitudinal Processes

AbstractIt is a common assumption that responses on implicit measures are proxies for automatically activated associations stored in memory. Consequently, explanations for implicit attitude malleability, variability, and prediction have assumed differences in underlying associations. However, a growing body of evidence challenges the assumption that implicit attitude change is driven only by associative processes. This paper reviews evidence from research with the Quadruple Process model on the influence of associative and non‐associative processes on implicit task performance. We also describe recent research on non‐attitudinal processes that do not pertain directly to the attitude object of interest but that, nevertheless, influence implicit task performance. Implications for the interpretation of implicit measures and implicit attitude change are discussed.

A further assessment of the Hall–Rodriguez theory of latent inhibition.

The Hall-Rodriguez (G. Hall & G. Rodriguez, 2010, Associative and nonassociative processes in latent inhibition: An elaboration of the Pearce-Hall model, in R. E. Lubow & I. Weiner, Eds., Latent inhibition: Data, theories, and applications to schizophrenia, pp. 114-136, Cambridge, England: Cambridge University Press) theory of latent inhibition predicts that it will be deepened when a preexposed target stimulus is given additional preexposures in compound with (a) a novel stimulus or (b) another preexposed stimulus, and (c) that deepening will be greater when the compound contains a novel rather than another preexposed stimulus. A series of experiments studied these predictions using a fear conditioning procedure with rats. In each experiment, rats were preexposed to 3 stimuli, 1 (A) taken from 1 modality (visual or auditory) and the remaining 2 (X and Y) taken from another modality (auditory or visual). Then A was compounded with X, and Y was compounded with a novel stimulus (B) taken from the same modality as A. A previous series of experiments (H. T. Leung, A. S. Killcross, & R. F. Westbrook, 2011, Additional exposures to a compound of two preexposed stimuli deepen latent inhibition, Journal of Experimental Psychology: Animal Behavior Processes, Vol. 37, pp. 394-406) compared A with Y, finding that A was more latently inhibited than Y, the opposite of what was predicted. The present experiments confirmed that A was more latently inhibited than Y, showed that this was due to A entering the compound more latently inhibited than Y, and finally, that a comparison of X and Y confirmed the 3 predictions made by the theory.

Renewal and reinstatement of the conditioned but not the unconditioned response following habituation of the unconditioned stimulus

Research on the inhibition of learned fear currently relies almost exclusively on one specific procedure, namely extinction of the conditioned stimulus (CS). Importantly, however, learned fear responses can be reduced by a number of other procedures, including habituation of the unconditioned stimulus (US). We recently demonstrated that reductions in learned fear following US habituation, like CS extinction, were subject to both renewal and reinstatement (Storsve et al., 2010). The present study further investigates the associative and non-associative processes shared between habituation and extinction. Given that habituation is typically context-independent (Mackintosh, 1987), in the present study we directly compared renewal and reinstatement of both a conditioned response (CR; freezing) and an unconditioned response (UR; startle) following habituation. It was found that the reduction in conditioned freezing resulting from habituation was context specific (i.e., a change in context led to a renewal of the conditioned fear response; Experiment 1) and was attenuated when a pre-test shock was given (i.e., reinstatement of conditioned fear was observed; Experiment 2). In contrast, habituation of an unconditioned response elicited by the US (i.e., a startle response) was unaffected by either a change in test context or administration of a pre-test shock. This dissociation in the effects of habituation on learned and unlearned responses is discussed in relation to theories of fear extinction.

MK-801 induces a low intensity conditioned taste aversion

N-methyl-d-aspartate (NMDA) receptor antagonists are often used to assess the role of NMDA receptors in learning and memory processes. However, few studies have explored the possibility that the antagonists may induce a conditioned aversion when administered following flavor consumption. We report five experiments with rats intended to evaluate the MK-801 capacity to induce conditioned taste aversion. Our findings suggest that: i) MK-801 produces a low-intensity aversion following repeated pairings with saccharin (Experiments 1 and 2); ii) such aversion was not the result of a non-associative process (Experiment 3); and iii) pre-exposure to MK-801 does not interact with conditioned taste aversion induced by lithium chloride (Experiments 4 and 5). These findings suggest that MK-801 induces a low-intensity aversion, although the underlying mechanisms of this aversion may differ from those of a conditioned aversion produced by lithium chloride.

Neurobehavioural plasticity

Neurobehavioural plasticity

Chemosensory conditioning in molluscs: II. A critical review

We critically review chemosensory conditioning studies with molluscs and find that, in many studies, the influence of nonassociative processes complicates, obscures, and renders ambiguous the unique contribution of associative learning. These nonassociative processes include sensory adaptation, habituation, sensitization, and changes in feeding motivation. They arise from both the food extracts that have often been used as conditioned stimuli and the aversive stimuli that have been used as unconditioned stimuli.

Chemosensory conditioning in molluscs: I. Failure of contextual conditioning inHermissenda

Aversive chemosensory conditioning alters Hermissenda's feeding behavior. But opposite behavioral changes have been reported, depending on whether discrete-trial or context-conditioning paradigms were used, raising questions about the roles of associative and nonassociative processes. We attempted to produce chemosensory contextual conditioning but failed to do so across a wide range of conditions. In Experiments 1-3, we observed large, nonspecific bite latency increases to shellfish extracts, regardless of whether they had signaled the presence or absence of shaking. In Experiment 4, we found that mere exposure to shellfish extract produced latency increases; vestibular stimulation was unnecessary. In a final experiment, using Y-maze choice tests, we failed to observe selective reductions in animals' preference for shellfish paired with shaking. Nonassociative processes stemming from prolonged exposure to concentrated shellfish extracts appear to be major factors in our failure to demonstrate associative chemosensory contextual conditioning.

Learning modulates the ensemble representations for odors in primary olfactory networks.

Recent evidence suggests that odor-driven responses in the insect antennal lobe (AL) can be modified by associative and nonassociative processes, as has been shown in the vertebrate olfactory bulb. However, the specific network changes that occur in response to olfactory learning remain unknown. To characterize changes in AL network activity during learning, we developed an in vivo protocol in Manduca sexta that allows continuous monitoring of neural ensembles and feeding behavior over the course of olfactory conditioning. Here, we show that Pavlovian conditioning produced a net recruitment of responsive neural units across the AL that persisted after conditioning. Recruitment only occurred when odor reliably predicted food. Conversely, when odor did not predict food, a net loss of responsive units occurred. Simultaneous measures of feeding responses indicated that the treatment-specific patterns of neural recruitment were positively correlated with changes in the insect's behavioral response to odor. In addition to recruitment, conditioning also produced consistent and profound shifts in the temporal responses of 16% of recorded units. These results show that odor representations in the AL are dynamic and related to olfactory memory consolidation. We furthermore provide evidence that the basis of the learning-dependent changes in the AL is not simply an increase in activity in the neural network representing an odorant. Rather, learning produces a restructuring of spatial and temporal components of network responses to odor in the AL.

An extinction cue reduces spontaneous recovery of ataxic ethanol tolerance in rats.

Ethanol ataxia experiments with rats investigated cue effects on conditioned tolerance. Spontaneous recovery (SR) was assessed 1 day and 18 days after extinction with conditioned stimuli (CSs) paired or unpaired with an ethanol unconditioned stimulus (US). Behavioral tolerance was assessed by not tilting the apparatus during conditioning. Non-associative processes were assessed post-conditioning with or without a buzzer cue. Bouton's (1993, Psychol Bull 114:80-99) memory theory was tested using an extinction cue and an associatively neutral cue presented during SR testing. Tolerance was conditioned to a room + strobelight CS by ethanol injections experienced on a tilting floor (standard conditioning). Controls received no ethanol or ethanol, either during the CS without the floor tilting or 11 h post-CS. SR testing occurred 1 day or 18 days after extinction (experiment 1). Conditioning was followed by tolerance and CR tests either with or without a 15-s buzzer cue (experiment 2). In extinction, the CS and cue occurred without ethanol; the cue occurred before 7% or none of the extinction trials. Testing occurred 18 days after extinction with or without that cue (experiment 3), or with an equally familiar ("neutral'') cue presented before conditioning (experiment 4). Tolerance developed without floor tilting. CS-US unpairings prevented tolerance. Tolerance SR occurred 18 days but not 1 day after extinction only after CS-US pairings (experiment 1). Post-conditioning tests showed no unconditioned effects of the cue (experiment 2). Testing with no cue 1 day after extinction with the cue resulted in no tolerance increase. The extinction cue reduced SR (experiments 3 and 4); the neutral cue did not (experiment 4). Cues correlated with extinction reduce SR. Non-associative and practice processes, Bouton's (1993, Psychol Bull 114:80-99) memory theory, alternative interpretations, and clinical implications are discussed.

Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain.

The induction of associative synaptic plasticity in the mammalian central nervous system classically depends on coincident presynaptic and postsynaptic activity. According to this principle, associative homosynaptic long-term potentiation (LTP) of excitatory synaptic transmission can be induced only if synaptic release occurs during postsynaptic depolarization. In contrast, heterosynaptic plasticity in mammals is considered to rely on activity-independent, non-associative processes. Here we describe a novel mechanism underlying the induction of associative LTP in the lateral amygdala (LA). Simultaneous activation of converging cortical and thalamic afferents specifically induced associative, N-methyl-D-aspartate (NMDA)-receptor-dependent LTP at cortical, but not at thalamic, inputs. Surprisingly, the induction of associative LTP at cortical inputs was completely independent of postsynaptic activity, including depolarization, postsynaptic NMDA receptor activation or an increase in postsynaptic Ca2+ concentration, and did not require network activity. LTP expression was mediated by a persistent increase in the presynaptic probability of release at cortical afferents. Our study shows the presynaptic induction and expression of heterosynaptic and associative synaptic plasticity on simultaneous activity of converging afferents. Our data indicate that input specificity of associative LTP can be determined exclusively by presynaptic properties.