Latent inhibition and context change in psychometrically defined schizotypy

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Abstract

The disruption of latent inhibition within the schizophrenia spectrum has often been interpreted either as a result of increased attentional distractibility (attentional account) or as a result of deficient interference of past associations (associative account). The aim of the present investigation was to test competing predictions, as derived from the above theoretical accounts. In a visual search paradigm of latent inhibition, accuracy was examined as a function of prior experience with the target, and psychometrically defined schizotypy. In Experiment 1 (N=60), no context change was introduced. In accord with past evidence, latent inhibition was found to be intact in low-, but disrupted in high-schizotypy scorers, a result predicted both by attentional and associative accounts. In Experiment 2 (N=60), a context change was introduced. As predicted by past evidence, latent inhibition was disrupted in low-schizotypy scorers. However, latent inhibition was found to be intact in high-schizotypy scorers, a finding accommodated by attentional, but not associative accounts. Theoretical implications and alternative interpretations are also considered.

Introduction

Non-reinforced, pre-exposure to a stimulus CSPE results in retardation of subsequent conditioning to that stimulus, as compared to a non-pre-exposed stimulus CSNPE. This phenomenon (CSPE  US < CSNPE  US) is known as the stimulus pre-exposure effect, or latent inhibition (Lubow, 1989). It has been suggested (Lubow & Gewirtz, 1995) that repeated, non-reinforced pre-exposure makes a stimulus irrelevant, and, therefore, it is difficult for the participants to associate subsequently this pre-exposed stimulus CSPE with the presence of an important event, such as an unconditioned stimulus (US).

Three main sources of evidence suggest a link between latent inhibition and schizophrenia. Firstly, latent inhibition has been found to be disrupted, or attenuated, in schizophrenic patients (Baruch, Hemsley, & Gray, 1988a; Gray, Pilowsky, Gray, & Kerwin, 1995; Lubow, Kaplan, Abramovich, Rudnick, & Laor, 2000; but see Swerdlow, Braff, Hartson, Perry, & Geyer, 1996; Williams et al., 1998), in that performance (in either rule-learning or visual search paradigms) dependent upon a pre-exposed target CSPE tended to approximate the level of a non-pre-exposed target CSNPE. Secondly, in line with dimensional views of psychosis (Claridge & Broks, 1984; Eysenck & Eysenck, 1975), latent inhibition was found to be attenuated in non-clinical participants who score highly on psychometric measures of schizotypy (Allan, Williams, Wellman, & Tonin, 1995; Baruch, Hemsley, & Gray, 1988b; Braunstein-Bercovitz & Lubow, 1998; Hofer, Della Casa, & Feldon, 1999; Lipp & Vaitl, 1992; Lubow, Ingberg-Sachs, Zalstein-Orda, & Gewirtz, 1992; Tsakanikos, Sverdrup-Thygenson, & Reed, 2003), suggesting that this phenomenon might constitute a marker for schizophrenia. A third source of evidence comes from psychopharmacological studies given that antipsychotic agents have been found to restore selectively the amphetamine-induced disruption of latent inhibition (see, Moser, Hitchcock, Lister, & Moran, 2000; Weiner et al., 2000, for reviews). The above evidence, taken together, and coupled with the fact that latent inhibition can be induced in both humans and non-humans, has led investigators to treat latent inhibition as a keystone for understanding putative neuropsychological systems that are implicated in schizophrenia (Gray, 1998; Weiner, 1990). Consequently, latent inhibition has been established during the last decade as a widely employed animal model of schizophrenia (for reviews see Escobar, Oberling, & Miller, 2002; Moser et al., 2000; Weiner et al., 2000).

Despite the established link between latent inhibition and psychosis, the theoretical basis of this phenomenon remains controversial, making the interpretation of this relationship equivocal. For example, there is little agreement on the specific nature of the deficit implicated in the disruption of latent inhibition in schizophrenia and in schizotypy.

Two main sets of theories1 have been proposed to explain the disruption of latent inhibition in schizophrenia. The first set of theories can be described as attentional. Attentional theories are based on the premise that latent inhibition is the result of the inability of the pre-exposed stimuli to elicit an attentional response (Lubow, 1989; Mackintosh, 1975). According to this view, disruption of latent inhibition can be explained in terms of an increased distractibility that characterizes schizophrenic patients. Due to this putative distractibility, schizophrenic patients fail to ignore irrelevant stimuli, and conditioning to a pre-exposed (and, therefore, supposedly irrelevant) stimulus progresses at the same rate as to a non-pre-exposed stimulus (Braunstein-Bercovitz & Lubow, 1998). This attentional account on latent inhibition deficits is further supported by evidence on impaired performance in schizophrenic patients in various paradigms of selective attention (see, Braff, 1993; Nestor & O’Donnell, 1998, for reviews).

The second set of latent inhibition theories can be described as associative. Associative theories (e.g., Reed & Tsakanikos, 2002; Weiner, 1990; see also Pearce & Bouton, 2000) are based on the assumption that stimulus––no event associations are formed during the pre-exposed phase (Phase I) that subsequently interfere with conditioning to the CSPE during the testing phase (Phase II). In accord with the associative view, albeit from a cognitive perspective, latent inhibition has been explained as the result of past regularities (i.e. ‘the CSPE does not predict a significant event’), which interferes later on with the acquisition of new information about the CSPE (Hemsley, 1993).

According to the associative account, schizophrenic patients fail to retain (or to retrieve) past associations from the pre-exposure phase. Therefore, in the absence of any associative interference, conditioning to the CSPE tends to progress at the same rate as for the CSNPE (for a review see Escobar et al., 2002). The associative interpretation is consistent with evidence on short-term memory and learning deficits in schizophrenia (Hofer, Doby, Anderer, & Dantendorfer, 2001; Goldberg, Patterson, Taqqu, & Wilder, 1998), and in psychometrically defined schizotypy (Lenzenweger, 2000; Tallent & Gooding, 1999), given that such deficits could account for a potential failure to retain (or to retrieve) the past associations required for the development of latent inhibition.

In latent inhibition studies, the term ‘context’ typically refers to the surrounding environmental stimuli (or the apparatus) within which the stimulus pre-exposure takes place. Latent inhibition is a context-dependent effect, because the introduction of a context change from the pre-exposure to the testing phase has been shown to disrupt or reduce latent inhibition in both humans (Gray et al., 2001; Kaplan & Lubow, 2001; Zalstein-Orda & Lubow, 1995) and non-humans (Lubow, Rifkin, & Alec, 1976).

Given this context dependency, a general convention of generating latent inhibition requires presentation of the target CSPE with pre-exposed (familiar) distracters, which is though to constitute part of a stable context (Lubow, 1997). Consistent with this view, in a two-experiment investigation (Gibbons & Rammsayer, 2001), it has been shown that presenting a target CSPE in the context of novel distracters during the testing phase (Experiment 2), as compared to familiar distracters (Experiment 1), attenuates latent inhibition in a visual search paradigm.

Despite the reported problems in context processing in schizophrenia (Cohen, Barch, Carter, & Servan-Schreiber, 1999; Cohen & Servan-Schreiber, 1992; Silverstein, Kovacs, Corry, & Valone, 2001; but see Bazin & Perruchet, 1996; Gold et al., 2000), a manipulation on the context of latent inhibition has never been investigated within the schizophrenia spectrum.

Importantly, the introduction of a context change could be used to test competing predictions derived from different theoretical accounts regarding the disruption of latent inhibition in schizotypy. According to the associative account, high-schizotypy scorers would fail to demonstrate latent inhibition independently of a context change. A disrupted latent inhibition would be expected for high-schizotypy scorers both within a stable context, and after a context change. However, according to the attentional interpretation, latent inhibition in high-schizotypy scorers would be disrupted only within a stable context (target pre-exposed/distracters pre-exposed). On the contrary, a context change (target pre-exposed/distracters non-pre-exposed) could restore latent inhibition in high-schizotypy scorers.

This latter prediction is derived from the attentional interpretation of the latent inhibition deficits, according to which high-schizotypy scorers are particularly distracted by irrelevant stimuli/distracters, coupled with evidence that novelty automatically captures attention during visual search (Johnston & Hawley, 1994). This attentional bias to novelty over familiarity (novel pop-out) has been shown to the same extent in both schizophrenic and non-clinical participants (Lubow et al., 2000), therefore, novelty per se would not have a differential impact on performance for high-, as compared to low-, schizotypy scorers. Nevertheless, the additive effects of irrelevance and novelty in the surrounding distracters (context change) during the testing phase would reinstate latent inhibition for high-schizotypy scorers. Because of the putative attentional distractibility, and given the attentional bias to novelty, it would be expected that novel irrelevant stimuli/distracters would provide the high-schizotypy scorers with a more effective distraction from the familiar target CSPE during the testing phase, as compared to a novel target CSNPE. Consequently, the context change (novel + irrelevant stimuli) would distract attention from the familiar target CSPE during the testing phase, ‘reinstating’ latent inhibition (CSPE  US < CSNPE  US).

The aim of the present investigation was to test the above competing predictions in a visual search paradigm of latent inhibition. In both experiments, accuracy was investigated as a function of pre-exposure to the target and schizotypy level. In Experiment 1, the context remained stable (familiar distracters) throughout the experiment. In Experiment 2, a context change (novel distracters) was introduced in the testing phase.

Section snippets

Experiment 1

Experiment 1 was based on a variation of a visual search paradigm of latent inhibition (Tsakanikos et al., 2003). The procedure consisted of two phases: a masked pre-exposure (see Lubow & Gewirtz, 1995, for a discussion) and testing phase. In the pre-exposure phase, all the participants were presented with fast moving round blocks of various colours, and were asked to make judgments in terms of their relative speeds. During this phase, participants in the experimental condition (pre-exposed/PE)

Experiment 2

In line with past evidence, latent inhibition was found to be disrupted for high-schizotypy scorers as compared to low-schizotypy scorers in Experiment 1. However, a disruption of latent inhibition in high-schizotypy scorers could be explained both by associative and attentional theories (see Section 1), making equivocal any interpretation of this performance deficit. Therefore, in Experiment 2, a context change will attempt to test opposite predictions as derived from the two main sets of

General discussion

In Experiment 1, latent inhibition was disrupted for high-schizotypy scorers, but was intact for low-schizotypy scorers, replicating past studies that employed a similar procedure (Tsakanikos et al., 2003), as well as various other experimental paradigms (Allan et al., 1995; Baruch et al., 1988b; Braunstein-Bercovitz & Lubow, 1998; Hofer et al., 1999; Lipp & Vaitl, 1992; Lubow et al., 1992).

In Experiment 2, a context change was introduced. This context change had a detrimental effect on latent

Acknowledgements

Thanks are due to Wing Yi Cheng, Chin Chin Esther Chan, Wing Chi Mak, Michelle Yip, Katy Robjant and Rory Trawber, for their help with the data collection, and three anonymous reviewers for their helpful comments and suggestions on an earlier version of the manuscript.

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