Visual search in scenes involves selective and nonselective pathways

How does one find objects in scenes? For decades, visual search models have been built on experiments in which observers search for targets, presented among distractor items, isolated and randomly arranged on blank backgrounds. Are these models relevant to search in continuous scenes? This article argues that the mechanisms that govern artificial, laboratory search tasks do play a role in visual search in scenes. However, scene-based information is used to guide search in ways that had no place in earlier models. Search in scenes might be best explained by a dual-path model: a 'selective' path in which candidate objects must be individually selected for recognition and a 'nonselective' path in which information can be extracted from global and/or statistical information.     

Interference and the representation of order within associations

In the presence of interference, recall of pairs can critically depend on the diagnostic power of memory of the order of items within the pair. Models of pair memory make different assumptions about whether and how such order information is stored, from convolution-based models, which assume no explicit storage of order, to matrix models and several models that assume a pair is learned by concatenating the representations of the constituent items, which lead to perfect within-pair order memory (given retrieval of the pair). Here we investigate memory for associations and within-pair order by examining the relationship between forward and backward probes of pairs subject to order-dependent associative interference in a double-function list paradigm. Associative interference disrupted the high correlation between forward and backward recall accuracy that is typically observed in standard paired-associate learning, challenging matrix and concatenation-based models. However, participants could overcome some interference due to within-pair order ambiguity, challenging directionally ambiguous convolution-based models. Unexpectedly, the test-retest correlation was reduced for pairs under the influence of interference compared to control pairs. This finding is incompatible with all existing implementations of the model classes we consider. Any model must include an assumption that order encoding (but not retrieval) is unreliable, and the form of this additional mechanism may depend intimately on how a given model is designed. In sum, our findings suggest that within-pair order memory is neither poor nor perfect, pointing to a fallible mechanism for within-pair order learning in verbal association-memory tasks.     

Increases in rewards promote flexible behavior

Offering reward for performance can motivate people to perform a task better, but better preparation for one task usually means decreased flexibility to perform different tasks. In six experiments in which reward varied between low and high levels, we found that reward can encourage people to prepare more flexibly for different tasks, but only as it increased from the level on the previous trial. When the same high rewards were offered continuously trial after trial, people were more inclined to simply stick with doing what had worked previously. We demonstrated such enhancements in flexibility in task switching, a difficult visual search task, and an easier priming of pop-out search task, which shows that this effect generalizes from executive tasks to perceptual processes that require relatively little executive control. These findings suggest that relative, transient changes in reward can exert more potent effects on behavioral flexibility than can the absolute amount of reward, whether it consists of money or points in a social competition.     

Lifelong reductions of PKMζ in ventral hippocampus of nonhuman primates exposed to early-life adversity due to unpredictable maternal care

Protein kinase Mζ (PKMζ) maintains long-term potentiation (LTP) and long-term memory through persistent increases in kinase expression. Early-life adversity is a precursor to adult mood and anxiety disorders, in part, through persistent disruption of emotional memory throughout life. Here we subjected 10- to 16-wk-old male bonnet macaques to adversity by a maternal variable-foraging demand paradigm. We then examined PKMζ expression in their ventral hippocampi as 7- to 12-yr-old adults. Quantitative immunohistochemistry reveals decreased PKMζ in dentate gyrus, CA1, and subiculum of subjects who had experienced early-life adversity due to the unpredictability of maternal care. Adult animals with persistent decrements of PKMζ in ventral hippocampus express timid rather than confrontational responses to a human intruder. Persistent down-regulation of PKMζ in the ventral hippocampus might reduce the capacity for emotional memory maintenance and contribute to the long-lasting emotional effects of early-life adversity.

Early-life adversity is associated with an increased vulnerability to stress-related disorders that is maintained into adulthood, suggesting a very long-lived effect on emotional memory by the early-life event (Coplan et al. 1996). Although several structural and neurochemical sequelae of early-life adversity have been reported (Teicher et al. 2003; Jackowski et al. 2011), the direct effects of early-life adversity on the molecular substrates maintaining long-term memory storage have not been explored.Accumulating evidence supports a crucial role for the autonomously active, atypical protein kinase C (PKC) isoform protein kinase Mζ (PKMζ) in maintaining synaptic long-term potentiation (LTP), a putative physical substrate for memory, and long-term memory storage (Ling et al. 2002; Pastalkova et al. 2006; Glanzman 2013; Sacktor and Fenton 2018). The autonomous activity of PKMζ is due to its unusual structure that differs from other PKC isoforms (Sacktor et al. 1993). Most PKCs consist of two domains: a catalytic domain and an autoinhibitory regulatory domain that suppresses the catalytic domain. Therefore, most PKCs are inactive until second messengers bind to the regulatory domain and induce a conformational change that releases the autoinhibition. Because second messengers that activate PKCs such as Ca²⁺ or diacylglycerol have short half-lives, most PKCs are only transiently activated.PKMζ, in contrast, consists of an independent PKCζ catalytic domain, and the absence of an autoinhibitory regulatory domain results in autonomous and thus persistent activity once the kinase is synthesized. PKMζ mRNA is transcribed from an internal promoter within the PKCζ/PKMζ gene that is active only in neural tissue (Hernandez et al. 2003). The mRNA is translationally repressed and transported to dendrites of neurons (Muslimov et al. 2004). High-frequency afferent synaptic activity during LTP induction or learning derepresses PKMζ mRNA translation, triggering new synthesis of PKMζ protein (Osten et al. 1996; Hernandez et al. 2003; Tsokas et al. 2016; Hsieh et al. 2017).Once increased, the steady-state amount of PKMζ remains elevated during LTP or long-term memory maintenance. Recent work with quantitative immunohistochemistry (IHC) shows that spatial conditioning induces persistent increases of PKMζ in somatic and selective dendritic compartments of dorsal hippocampal CA1 pyramidal cells that can last at least 1 mo (Hsieh et al. 2021). The persistent increases are preferentially expressed in CA1 pyramidal cells that were activated during the formation of the memory, specifically at the termination zone of the Schaffer collateral/commissural inputs from subfield CA3. In contrast, persistent PKMζ increases are not evident in stratum lacunosum-moleculare, the termination zone that originates in entorhinal cortex that nonetheless is capable of expressing PKMζ. Postsynaptic domain-specific PKMζ expression patterns hint at distinct circuit-specific modifications of cortical–hippocampal synaptic function by maturational and experiential factors.Persistent changes in PKMζ expression are also associated with changes in the capacity for learning and memory across the life span of animals. Decreased memory ability in aged rats is associated with decreased training-induced, persistent PKMζ expression in prelimbic cortex, and increases in PKMζ are crucial for the cognition-enhancing effects of environmental enrichment in the aged animals (Chen et al. 2016). Hara et al. extended the connection between PKMζ and cognitive function to nonhuman primates (NHPs), showing that levels of PKMζ expression in dentate gyrus (DG) axospinous synapses correlate with successful performance on cognitive tasks in young and aged monkeys (Hara et al. 2012). These studies suggest that persistent down-regulation of PKMζ may comprise an important pathophysiological mechanism for cognitive impairment.Here we used a validated NHP model of early-life adversity, maternal variable-foraging demand (VFD), to explore the links between adversity in infancy and PKMζ expression in adulthood (Coplan et al. 1996; Jackowski et al. 2011). Previous studies of the VFD paradigm have revealed that both infants and their mothers exposed to VFD show significant cerebrospinal fluid (CSF) elevations of the stress neuropeptide, corticotropin-releasing factor (CRF). Moreover, the magnitude of CRF change in mothers and infants are positively correlated, suggesting synchronization of maternal–infant stress responses to the VFD stressor (Coplan et al. 2005). From a behavioral standpoint, maternal social rank plays a negligible role in determining an aggregate score of maternal–infant proximity, suggesting preferential attention of mothers to their infants. During the VFD condition, maternal social rank predicts >80% of the variance of maternal–infant proximity, suggesting mothering patterns are interrupted by preferential orientations to social rank; the latter determines food accessibility (Coplan et al. 2015). Dominant females show relative increases in maternal–infant proximity, whereas subordinate females show relative reductions in maternal–infant proximity. Neither pattern of attachment ameliorates an abnormal association between CSF oxytocin concentrations and hypothalamic-pituitary-adrenal (HPA) axis activity (Coplan et al. 2015). Offspring exposed to VFD rearing assessed both as juveniles and as full adults demonstrate persistent increases in CSF CRF concentrations in comparison with controls reared under non-VFD conditions (Coplan et al. 1996, 2001).Our prior neurohistological studies pointed to the DG as a region particularly vulnerable to VFD exposure, as shown by reduced trophic signaling and neurogenesis (Jackowski et al. 2011; Perera et al. 2011; Schoenfeld et al. 2021). We therefore hypothesized that early-life adversity due to unpredictable maternal care (for brevity, subsequently referred to as “early-life adversity”) reduces the persistent expression of PKMζ within the DG of ventral intrahippocampal neurocircuitry that mediates affective memory processing (Fanselow and Dong 2010). We used PKMζ antisera validated by the lack of immunostaining in PKMζ-null mice (Hsieh et al. 2021) to examine PKMζ expression in ventral hippocampus (NHP anterior hippocampus) in both DG granule cell layer and the stratum moleculare of the suprapyramidal blade that receives direct input from entorhinal cortex, as well as other regions encompassing the hippocampal formation, including the hilus, CA3, CA1, and subiculum.To assess behavioral correlates of hippocampal PKMζ expression, we used a stress-inducing paradigm designed specifically for singly housed bonnet macaque male NHPs, which we refer to as the “human exposure response” (Jackowski et al. 2011; Hamel et al. 2017), which is a variation of the paradigm used in human exposure studies by Kalin et al. in rhesus macaques (Kalin and Shelton 1989). On exposure to a direct human presence, singly housed adult male bonnet macaques react with a dichotomy of responses—confrontational versus timid (see the Materials and Methods) (Jackowski et al. 2011). In our macaque colony, groups of fully adult males are necessarily housed individually to prevent injury sustained during male agonistic encounters, whereas adult females and/or juveniles are safely housed in social groups. Because group housing of nursing females and/or juveniles of both sexes elicits a range of behaviors intrinsic to the species’ social repertoire (Rosenblum et al. 2001; Coplan et al. 2015) that complicates behavioral analyses to human exposure, we restricted our current study to male macaques.     

Linking associative and serial list memory: Pairs versus triples

Paired associates and serial list memory are typically investigated separately. An "isolation principle" (J. B. Caplan, 2005) was proposed to explain behavior in both paradigms by using a single model, in which serial list and paired associates memory differ only in how isolated pairs of items are from interference from other studied items. In the present study, 2 experiments identify a critical dissociation between the 2 paradigms, challenging this unified account. Specifically, forward and backward probes were highly correlated for pairs and less so for short lists (triples). The authors asked whether the isolation principle could quantitatively accommodate this type of dissociation. A simulation confirmed that a single model incorporating the isolation principle can adequately explain this and other dissociations, supporting the common processes view.     

Combining speed and accuracy to assess error-free cognitive processes

Both the speed and accuracy of responding are important measures of performance. A well-known interpretive difficulty is that participants may differ in their strategy, trading speed for accuracy, with no change in underlying competence. Another difficulty arises when participants respond slowly and inaccurately (rather than quickly but inaccurately), e.g., due to a lapse of attention. We introduce an approach that combines response time and accuracy information and addresses both situations. The modeling framework assumes two latent competing processes. The first, the error-free process, always produces correct responses. The second, the guessing process, results in all observed errors and some of the correct responses (but does so via non-specific processes, e.g., guessing in compliance with instructions to respond on each trial). Inferential summaries of the speed of the error-free process provide a principled assessment of cognitive performance reducing the influences of both fast and slow guesses. Likelihood analysis is discussed for the basic model and extensions. The approach is applied to a data set on response times in a working memory test. The authors wish to thank Roger Ratcliff, Christopher Chabris, and three anonymous referees for their helpful comments, and Aureliu Lavric for providing the data analyzed in this paper.     

Hemispheric cognitive style: a comparison of three instruments

In this study, the author tested the reliability, concurrent validity, and predictive validity of three hemispheric cognitive style instruments: (a) the Preference Test (PT; R. Zenhausern, 1978), (b) the Polarity Questionnaire (PQ; B. E. Morton, 2002), and (c) the Wagner Preference Inventory II (WAPI II; R. F. Wagner & K. A. Wells, 1985). Participants were either teachers or teachers in training. The prediction criterion was in the area of teaching licensure. Scores on the PQ had extremely low reliability, and correlations with the PT and the WAPI II were not significantly different from zero. In addition, the PQ did not correlate with the licensure area. The author found that both the PT and the WAPI II had reasonable levels of reliability, and both instruments were able to explain a small percentage of the variance in the teaching licensure area. Using factor analysis of the PT, the author found a 7-factor structure, which suggests that hemispheric cognitive style might be decomposable into separate holist analytic and visual-verbal dimensions.