Free recall of pleasant words from recency positions is especially sensitive to acute administration of cortisol

Psychoneuroendocrinology 29 (2004) 327–338 www.elsevier.com/locate/psyneuen

Free recall of pleasant words from recency positions is especially sensitive to acute administration of cortisol M. Tops a,b,∗, G. van der Pompe a,b, A.A. Wijers b, J.A. Den Boer a, T.F. Meijman b, J. Korf a a

Department of Psychiatry, University of Groningen and Graduate School of Behavioral and Cognitive Neurosciences, Grote Kruisstraat 2/1, 9712 TS Groningen, The Netherlands b Department of Experimental and Work Psychology, University of Groningen and Graduate School of Behavioral and Cognitive Neurosciences, Grote Kruisstraat 2/1, 9712 TS Groningen, The Netherlands Received 21 June 2002; received in revised form 21 November 2002; accepted 31 January 2003

Abstract In a recent study we investigated the acute effects of cortisol administration in healthy male volunteers on free recall of pleasant, unpleasant, and neutral nouns using a between-subjects double-blind placebo-controlled design. The volunteers were administered 10 mg of hydrocortisone or placebo between 9:00 and 10:30. Two hours after administration of cortisol a decline in recall of neutral and pleasant words was found, while recall of unpleasant words did not change. These results are consistent with a possible inhibitory influence of cortisol on a prefrontal dopaminergic mechanism involved in approach and positivity bias. In this paper we first explain why this interpretation would predict recall of pleasant words from recency positions to be especially sensitive to cortisol administration. Comparing primacy and recency recall of pleasant and unpleasant words, there proved to be a selective decline in recall of pleasant recency words. These results did not appear to stem from differences in recall strategies between our groups of volunteers.  2003 Elsevier Ltd. All rights reserved. Keywords: Cortisol; Serial position; Recency; Positivity bias; Verbal memory; Depression

∗

Corresponding author. Tel.: +3150-3636473; fax: +3150-3636304. E-mail address: [email protected] (M. Tops).

0306-4530/$ - see front matter  2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0306-4530(03)00032-5

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Nomenclature T N ⌺Ri

Total number of words recalled Number of recency words recalled Sum of the ranks of recency words(the first word output is given a rank of 1, the second 2, and so on)

1. Introduction Normally healthy subjects display recall of pleasant material that is superior to recall of unpleasant material (see for a meta-analysis Matt et al., 1992). This Pollyanna tendency or the tendency to utilize pleasant words over unpleasant words has been described by Boucher and Osgood (1969) as a stable cross-cultural phenomenon. This phenomenon is also referred to as a “positivity bias” in recall. Positivity bias and positive illusions are found to be a functional part of approach-related action-oriented thinking (e.g., Taylor and Gollwitzer, 1995). Approach motivation, action-oriented processing and the influence of mild positive affect on cognition are thought to be mediated by dopamine function in the mesocorticolimbic system (e.g., Ashby et al., 1999; Depue and Collins, 1999). In a previous paper (Tops et al., in press) we reported detrimental effects of cortisol administration on free recall and recognition of pleasant and neutral words by healthy volunteers, and no effects on memory for unpleasant words. The positivity bias in the recall by subjects who received a placebo was completely absent in the recall by subjects who received cortisol. This is particularly interesting because these results parallel the recall and recognition differences usually found in people suffering from depression (see for a meta-analysis Burt et al., 1995) and low approach motivation has been proposed to be a characteristic of depression (e.g., Depue and Iacono, 1989; Henriques and Davidson, 2000). There is substantial evidence to support the view that depression is associated with decreases in dopamine, although this hypothesis is not the only pharmacological explanation of depression that is supported in the literature (see Willner, 1985). In depression alterations in the cortisol hormonal system and high basal cortisol levels are often found (e.g., Gold et al., 1988). Sustained hypercortisolism also diminishes dopamine release in the nucleus accumbens of rats, an important component of the mesolimbic reward system; such an effect is likely to contribute to the anhedonia of depression (Imperato et al., 1993). The same pattern of significantly lower recall of pleasant material when compared to controls, and comparable memory for unpleasant material as controls, has been found in normals who had been administered the D2 dopamine receptor antagonist haloperidol (Kumari et al., 1998). Also, it is known that the mesocorticolimbic dopaminergic system is involved in the modulation of memory consolidation by glucocorticoids like cortisol (e.g., Roozendaal et al., 2001).

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Before proceeding with this introduction, the phenomenon of the serial position curve has to be considered. A serial position curve indicates the probability for each item of a list of items to be recalled as a function of its position in this list. A typical serial position curve shows an enhanced probability for the first few (primacy) and for the last few items (recency) of the list to be recalled (for a review see Glanzer, 1982). Initially serial position effects were interpreted in terms of a two-store model of memory processing, where the primacy effect was considered to represent long term processes, and the recency effect reflected working memory functions. In recent years several authors have reported dissociations between verbal working memory span and recency (see Baddeley and Hitch, 1993). Therefore recency observed during verbal immediate free recall is considered to reflect only certain subcomponents of working memory without being directly related to span. Animal research has lead Freeman et al. (1996) to propose that working or recency memory is mediated by a system (the “anterior circuit”) involving anterior cingulate cortex and medial dorsal thalamic areas. This high-capacity memory system encodes new inputs rapidly on first presentation and holds them in store for immediate use. The operation of this circuit is likely to contribute importantly in tasks that require subjects to make relatively short-term mnemonic temporal discriminations (discriminations based on time since an item was stored) (Freeman et al., 1996). This anterior system overlaps with a system also including perirhinal cortex which is proposed to support memory that is the automatic consequence of passive exposure to stimuli (Aggleton and Brown, 1999). This system, together with the amygdala, may encode the salience of itemspecific information (Dalrymple-Alford et al., 1999). The anterior circuit of Freeman and al. (1996) consists of structures that are involved in the mesocorticolimbic dopaminergic system. Other areas involved in this system are the ventral striatum (i.e., nucleus accumbens), ventral tegmental area, perirhinal, orbitofrontal and dorsolateral frontal cortex. Several of these areas may be involved in processes relevant to serial position. Single neurons in the monkey ventral striatum and perirhinal cortex signal progress through a sequence of epochs in which intermediate goals and rewards can be identified (Liu and Richmond, 2000; Shidara et al., 1998). Neurons in these areas carry strong signals about associative behavioral significance of stimuli related to the progress through a predictable schedule of trials. The monkeys of Lui and Richmond were most motivated during trials in which they knew the reward is forthcoming. The ventral striatum is well-placed to take part in planning and maintaining behavior in response to emotionally significant stimuli. Interestingly, it has even been found that primacy and recency items are rated as more pleasant, even when controlled for recall (Matlin, 1974, 1975; Stang, 1975). It may be that certain serial positions are intrinsically rewarding (Stang, 1975), as are pleasant stimuli. As evidenced from intracranial ERPs, the anterior dorsolateral and cingulate cortices were found to contribute to short-term memory and recency judgment (Guillem et al., 1996). Milner (1968) found that left dorsolateral frontal cortex lesions lead to a deficit in verbal recency tasks. One further central characteristic of the dorsolateral frontal lobe deficit seems to be the disruption of inhibitory control, resulting in a failure to inhibit previous memory contents; one effect of which is

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proactive interference. Increased proactive interference may result in decreased recency recall, as proactive interference builds up over trials in a list (Murdock, 1962). In a study with patients with Parkinson’s disease, Sagar et al. (1988) suggests that recency discrimination deficits and the impaired immediate recognition from recency positions they found are specific cognitive deficits in Parkinson’s disease that may be linked to subcortical dopaminergic deafferentation of the frontal lobes. Other researchers have provided evidence of impairment in patients with PD on tests traditionally associated with frontal lobe function including release from proactive interference (Guillem et al., 1996; Tweedy et al., 1982). In general, dopamine function is thought to be central in frontal cortical mediation of working memory (Miller, 2000). In contrast to the relationships between recency and frontal functions, the presence of the primacy effect, but not the recency effect, has been shown to depend on the integrity of the hippocampal formation (Kesner, 1985; Zola-Morgan and Squire, 1990). Results of a recent study by Lupien et al. (1999) suggest that prefrontal cortex relevant working memory is more sensitive than hippocampally relevant aspects of declarative memory to the acute elevations of cortisol. As suggested by Lupien et al. (1999), it is possible that the changes in performance with glucocorticoid administration involve a prefrontal dopaminergic mechanism. The diverse literature discussed above seems to converge on the hypothesis that the mesocorticolimbic dopaminergic system would promote both recall of pleasant stimuli and recall from recency positions. As a consequence, recall of pleasant stimuli from recency items may be a sensitive index to the functioning of this system. Although it is not possible to test directly our dopaminergic hypothesis with the current data set, the following prediction regarding cortisol’s effects on memory was derived: If, in our study, the absence of the positivity bias after cortisol administration indeed resulted from inhibition of dopaminergic function, then we would expect the differences in positivity bias between our groups of subjects to be most evident for recency items. We tested this prediction by reanalyzing our data (Tops et al., in press) taking serial positions into account. Since in our study, subjects were instructed to write down as many words as they could immediately after the presentation of each list of words, recall of recency items in our study may reflect the immediate use, recency memory system proposed by Freeman et al. (1996). We will also calculate and analyze a measure of the relative output order of recency items: the relative index of priority (RIP) score. The RIP score reflects the priority given to words in various positions in the list and indicates changes in recall strategies (Dalezman, 1976). A desirable characteristic of the RIP score is that it is invariant with the number of words recalled. It, therefore, allows for between subjects comparisons (Flores and Brown, 1974). There is strong evidence that in immediate recall recency depends on the adoption of a retrieval strategy that involves recalling the last items first (Baddeley and Hitch, 1993).

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2. Methods 2.1. Subjects Twenty-two healthy male students aged 18–27 (mean age = 21.18) who had been screened in a separate session to exclude psychiatric, metabolic, and neurological conditions participated in this study. All subjects read and signed an informed consent statement approved by the Ethical Committee at the department of psychology. 2.2. Procedure and tests Subjects were randomly assigned to either an experimental condition (n = 13) or a placebo condition (n = 9). The group participating in the experimental condition was enlarged because we wanted to perform a correlational analysis not reported here. At the start of the experiment (between 9:00 and 10:30) subjects in the experimental condition received a capsule containing hydrocortisone acetate (10 mg of hydrocortisone), whereas subjects in the control condition received a placebo (avicel capsule) double-blind orally. After 1 h in which they were allowed to read, subjects performed a number of tasks for 1 h and 20 min. The free recall task was performed 2 h after ingestion of the capsule. 2.2.1. Word lists The recall task consisted of two lists with pleasant words, two lists with unpleasant words, and four lists with neutral words. Each word list presented to the participants contained 11 words from only one valence category. This allowed us to look for serial position effects for each category of words. All lists were matched for frequency of written use and word length. The pleasant words were matched with the unpleasant words for intensity of valence. 2.2.2. Immediate free recall The subjects were given a clipboard with one sheet for every word list. For each subject, the order of presentation of lists and of the words within each list were randomly selected. Words were presented sequentially on the screen for two seconds and immediately replaced by the next word. Subjects were instructed to try and remember as many words as possible. Immediately after each list the subjects were given 90 s to write down as many words they could from the list, in any order. 2.3. Serial position analyses A binary code (score) was assigned to the data set: a 1 if recalled, a 0 if not recalled. To calculate the percentage of words recalled from one category (e.g., pleasant) and one serial position, the average of the score of that serial position from both lists of that category was calculated and multiplied by one hundred. To calculate the percentage of words recalled from one part of the serial position curve, the average of the scores of the first four serial positions (primacy) or of the last four serial

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positions (recency) from both lists of that category was calculated and multiplied by one hundred. As discussed elsewhere (Tops et al., in press), our neutral and affective stimuli differed in ‘semantic cohesion’ (inter-item associations) (Maratos et al., 2000), but the pleasant nouns did not differ from the unpleasant nouns in this respect. This diminishes the comparability of the neutral with the affective stimulus categories. For this reason we decided only to include the affective (pleasant and unpleasant) nouns in the present analysis. Other arguments in support of this decision are the findings by Rogers and Revelle (1998) that pleasant and neutral stimuli are processed more similarly compared to unpleasant stimuli, and our interest in recall of pleasant words compared to unpleasant words (positivity / negativity bias). 2.4. Output order The order in which words were recalled was analyzed to determine if the order differed between treatments. The order of recall is a measure of priority: words with a higher priority are recalled earlier in the output than are words of lower priority. The relative index of priority (RIP) was calculated for words from the recency part (last four positions) of the list (Flores and Brown, 1974). This index was calculated by the following formula: RIP = [N(T + 1) - 2⌺R i] / N(T - N). This index has a maximum value of 1, indicating maximum priority has been given to recency words (they are recalled first), and a minimum value of -1, indicating that minimum priority has been given to recency words (they are recalled last). A score of zero indicates chance priority. For more details on the stimuli or methods of this study we refer to Tops et al. (in press).

3. Results 3.1. Output order The average relative index of priority (RIP) scores and standard deviations are presented in Table 1. The RIP scores were analyzed using a repeated measures MANOVA with cortisol treatment as between-group factor and with word-type as Table 1 Average relative indices of priority (RIP) and standard deviations for recency items

RIP unpleasant words RIP pleasant words

Placebo

(Std.)

Treatment

(Std.)

0.62 0.56

0.52 0.33

0.48 0.39

0.46 0.44

A positive RIP score means a tendency to recall recency items in the first part of the output order. A negative RIP score means a tendency to recall recency items at the end of the output order.

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within-factor. The results show that there was a general tendency for subjects to recall recency items first. Although less priority was given to recency items by the subjects in the treatment group, no differences or interactions between the groups and word-types approached significance (ps ⬎ 0.30). These results suggest that the differences in recall performance between our groups were not associated with differences in the recall strategies. 3.2. Serial position recall To test for differences in free recall between the treatment group and the placebo group depending on serial positions, we performed a repeated measures MANOVA with cortisol treatment as between-group factor and with serial position (1, 2, 3, ...11) as within-subjects factor. There was a significant effect of serial position ( F(10,11) = 5.62, p = 0.002) with the serial position curve showing the usual quadratic function indicating a primacy effect and a recency effect (F(1,20) = 44.75, p ⬍ 0.001; Fig. 1). There turns out to be a significant interaction between group and serial position (F(10,11) = 3.88, p = 0.009). To study this interaction between group and serial position further, we compared the primacy effect with the recency effect as a function of group. We defined the primacy effect as the average recall of words from the first four serial positions, and we defined the recency effect as the average recall from the last four serial positions. We performed a repeated measures MANOVA with cortisol treatment as betweengroup factor and with word-type (pleasant vs unpleasant) and serial position (primacy vs recency) as within-factors. There was, as in our previously reported analysis (Tops et al., in press), a significant main group effect (F(1,20) = 3.66, p = 0.035) and a significant interaction between group and word-type (F(1,20) = 4.43, p = 0.024), reflecting the lower recall of pleasant words in the treatment group. Additionally, there was a significant interaction between word-type and serial position ((F1,20) = 4.35, p = 0.025) and an almost significant three-way interaction between group, word-type, and serial position (F(1,20) = 2.50, p = 0.065). Separate tests for primacy and for recency recall showed that primacy recall of pleasant words was significantly better than primacy recall of unpleasant words, demonstrating positivity bias in the

Fig. 1. Percentage of words recalled as a function of serial position. (a) unpleasant words (b) pleasant words (c) percentage of pleasant minus percentage of unpleasant words recalled. When this value is greater than zero this indicates a positivity bias in recall, values smaller than zero indicate a negativity bias.

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recall of primacy items (F(1,20) = 3.74, p = 0.034; Fig. 1c). Recency recall was better in the placebo group compared to the treatment group (F(1,20) = 3.03, p = 0.049). There was a significant interaction in recency recall between group and wordtype (F(1,20) = 9.51, p = 0.003). Subjects in the treatment group recalled fewer pleasant recency items compared to subjects in the placebo group (F(1,20) = 9.83, p = 0.003; Fig. 1b). Subjects in the treatment group recalled fewer pleasant recency items compared to unpleasant recency items, demonstrating a negativity bias (F(1,12) = 16.56, p = 0.001; Fig. 1c). No other differences or interactions were significant.

4. Discussion The results tend to support the hypothesis of a specific impairment by cortisol of recall of pleasant words presented in recency positions. Subjects in the treatment group recalled fewer pleasant words compared to subjects in the placebo group, but this was only true for words presented in recency positions. Differences in positivity bias between the two groups were only present for recency items, and these differences resulted from the differences in recall of pleasant words from recency positions. There were no differences between the groups or word types in relative index of priority scores, indicating that the differences in recall performance between our groups were not associated with differences in the recall strategies. Recently Lupien et al. (1999) found significant acute decremental effects of infusion of 600 µg/kg/hr of cortisol on a working memory task (Sternberg memorysearch task), without any significant effect on a declarative memory task (cued recall). According to their interpretation this suggests that aspects of prefrontal cortex-mediated working memory are more sensitive than declarative memory mediated by, e.g., the hippocampus to the acute elevations of cortisol. Impaired recency but unimpaired primacy supports this hypothesis. In both humans and infraprimates, the presence of the primacy effect, but not the recency effect, has been shown to depend on the integrity of the hippocampal formation (Kesner, 1985; Zola-Morgan and Squire, 1990). In contrast, as outlined in the introduction, the recency effect has been linked to frontal function. As stated, Lupien et al. (1999) found no acute decremental effects of infusion of cortisol on a declarative memory task (cued recall). However, the results of Lupien and colleagues (and also the immediate recall results from de Quervain et al., 2000) contrast with those of Kirschbaum et al. (1996) who, like Lupien et al. using a cued recall task and a roughly comparable dose of cortisol, did find a decreased declarative memory 1 h after cortisol administration. As a possible explanation for this discrepancy Lupien et al. point out that their declarative memory task used an intentional encoding of the information (explicit instructions), whereas the declarative memory task used by Kirschbaum et al. used an incidental (implicit) encoding (participants were not aware at the time of encoding that they would be asked to recall the words later). This explanation is in accordance with our results, since we found cortisol administration to preferentially impair recall of recency items; immediate recall of

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recency items is thought to involve incidental encoding (Baddeley and Hitch, 1993). Additionally, it has been found that pleasant events and moods are associated with the use of rapid, heuristic and relatively effortless information-processing strategies (see for a review Taylor, 1991). The selective impairment of recall of pleasant words from recency positions is compatible with the hypothesis that sustained, relatively high levels of cortisol inhibit dopaminergic activity involved in approach and positivity bias (Laborit, 1976; Tops et al., in press). As outlined in the introduction, recall of pleasant words from recency positions may be sensitive to mesocorticolimbic dopaminergic function. Dopaminergic innervations of the ventral striatum (i.e., nucleus accumbens) and projections from there to the prefrontal cortex are part of the mesocorticolimbic dopaminergic system. Increased or prolonged dopamine release within the nucleus accumbens in response to salient stimuli would be expected to maintain the current selection of stimuli for intensive processing (Gray et al., 1999). The prefrontal cortex is thought to contain mechanisms for maintaining goal-relevant information, a process that is part of working memory. Cortisol may directly inhibit this dopaminergic activity, or this inhibition may take place through facilitation of cholinergic or serotonergic activity (Depue and Spoont, 1986; Laborit, 1976; Hoebel et al., 1999). Sustained, relatively high levels of cortisol (relative to e.g., (nor)adrenaline) are associated with uncontrollable stressors (Levine et al., 1989) and temperamental inhibition (Stansbury and Gunnar, 1994). According to a review by Levine et al. (1989), perhaps the most important single psychological factor involved in modulating cortisol responses to aversive stimuli is the dimension of control; control being defined as the capacity to make active responses during the presence of an aversive stimulus. Frankenhaeuser’s (1986) “distress without effort” pattern similarly summarizes literature involving a passive coping mode associated with increased cortisol activity. This pattern is found in contexts of low control and helplessness, and may involve disengagement from the pursuit of goals (Frankenhaueser, 1986). Cortisol has been hypothesized to facilitate the functioning of systems involved in the inhibition of approach and active coping both in the case of uncontrollability and temperamental inhibition (Laborit, 1976; Brown et al., 1996; Stansbury and Gunnar, 1994). This may be an adaptive mechanism in which sustained high levels of cortisol have a feedback function signaling situations in which approach may not be productive or even dangerous. This idea may be seen as an extension of the role of stress-level cortisol in counterregulating acute bodily stress responses, preventing those responses from becoming harmful themselves (Munck et al., 1984). Extending this functionality to the behavioral domain, we suggest that sustained relatively high levels of cortisol may inhibit approach and acute active coping, preventing these behavioral responses from becoming harmful in situations of uncontrollability (see also Laborit, 1976). Although the cognitive effects of sustained cortisol disturbance in depression are likely to be quite different than the effects of acute alterations in normal individuals, the present discussion may be relevant to depression. As mentioned in the introduction, depression is often characterized by a reduced positivity bias, even negativity bias in implicit memory (see for a review Gotlib and Krasnoperova, 1998), reduced approach, decreases or alterations in dopamine function, and high basal cortisol lev-

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els. Sustained hypercortisolism also diminishes dopamine release in the nucleus accumbens of rats, an important component of the mesolimbic reward system; such an effect is likely to contribute to the anhedonia of depression (Imperato et al., 1993). The anterior cingulate cortex and (especially left) dorsolateral prefrontal cortex are among the structures most consistently showing reduced activity in depressed patients (Davidson et al., 2002). We suggest that the adaptive cognitive alterations associated with prolonged relative high cortisol levels (i.e., reduced positivity bias) may, when sufficiently repeated or sustained, predispose to the development of depression. This functional explanation fits well with the evolutionary explanation of depression as an adaptation to situations in which effort to pursue a major goal will likely result in danger, loss, bodily damage, or wasted effort. In such situations, pessimism, reduced initiative, and lack of motivation may give a fitness advantage by inhibiting certain actions (Nesse, 2000). Though intriguing, the results of this study are qualified by several limitations, including the small number of subjects. Additionally, only male subjects were included in this study. Also, the effects of cortisol on memory may vary by time of day (Lupien et al., 2002). While this study requires replication preferably employing a within-subject design, the results are encouraging and are presented here to prompt continued research on the role of cortisol in biopsychological studies of possible mechanisms of the pathogenesis of depression. Acknowledgements Parts of this research is supported by the Netherlands Concerted Research Action ‘Fatigue at work’ of the Netherlands Research Organization (NWO) (580-02.100D). The authors would like to thank two anonymous reviewers for valuable comments on preceding versions of this paper. References Aggleton, J.P., Brown, M.W., 1999. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci 22 (3), 425–489. Ashby, F.G., Isen, A.M., Turken, A.U., 1999. A neuropsychological theory of positive affect and its influence on cognition. Psychol. Rev 106 (3), 529–550. Baddeley, A.D., Hitch, G., 1993. The recency effect: Implicit learning with explicit retrieval? Mem. Cogn 21 (2), 146–155. Boucher, J., Osgood, C.E., 1969. The pollyanna hypothesis. J. Verb. Learn. Verb. Behav. 8 (1), 1–8. Brown, L.L., Tomarken, A.J., Orth, D.N., Loosen, P.T., Kalin, N.H., Davidson, R.J., 1996. Individual differences in repressive-defensiveness predicts basal salivary cortisol levels. J. Pers. Soc. Psychol. 70 (2), 362–371. Burt, D.B., Zembar, M.J., Niederehe, G., 1995. Depression and memory impairment: A meta-analysis of the association, its pattern, and specificity. Psychol. Bull 117 (2), 285–305. Dalezman, J.J., 1976. Effects of output order on immediate, delayed, and final recall performance. J. Exp. Psychol.: Hum. Learn. Mem 2, 597–608. Dalrymple-Alford, J.C., Gifkins, A.M., Christie, M.A., 1999. Raising the profile of the anterior thalamus. Behav. Brain Sci 22 (3), 447–448.

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