Unexpected novelty and familiarity orienting responses in lateral parietal cortex during recognition judgment
Highlights
► Violation of memory expectations activate posterior parietal cortex. ► Left posterior parietal cortex demonstrates functional heterogeneity in orienting responses. ► Left anterior IPS/post-central gyrus selectively responds to unexpected novelty. ► Left anterior angular gyrus selectively responds to unexpected familiarity.
Introduction
The parietal lobe, particularly the posterior parietal cortex (PPC) has recently become the focus of a great deal of attention from memory researchers. This interest arose because the PPC is frequently activated in neuroimaging studies of recognition memory despite its more established role in visuo-spatial attention. However, parietal lesions are not historically linked with recognition memory impairment nor do recent neuropsychological investigations specifically examining basic recognition memory following parietal lesion suggest a discernible accuracy impairment memory, despite using tasks quite similar to those shown to activate lateral parietal areas during fMRI research (Ally et al., 2008, Ciaramelli et al., 2010, Dobbins et al., 2012, Simons et al., 2010). The inconsistency between the brain imaging and neuropsychological findings has continued to pique interest in the functional significance (if any) of the prominent activations seen in this region during recognition memory judgments.
In considering putative functional roles for the PPC, Wagner, Shannon, Kahn and Buckner (2005) reviewed neuroimaging studies that found PPC activation and noted that while the PPC tends to show an old-new effect (greater activity at retrieval for previously studied materials than previously unstudied materials), it was also sensitive to the subjective feeling of oldness (false alarms evoked more activity than misses), introspective indications of recollection vs. familiarity, and the goals or retrieval orientation of the participant. Following these observations and consideration of the role of the PPC in other research, they suggested three potential functions. First, the PPC could be involved in maintaining or shifting attention to “internal, mnemonic representations”. Under this account, when a participant retrieves information (presumably within another region, such as the medial temporal lobes (MTL)), the parietal lobe would be needed to move attention from external stimuli, or other memory representations, to this new memory content. Second, the PPC could be a “mnemonic accumulator”, gathering episodic memory evidence from other regions in service of making an eventual memory decision. The portions of PPC connected to the MTL, for example, could integrate its retrieval activity over time, triggering a judgment of recognition when information levels reached a decision bound. Finally, the PPC could be an episodic memory output buffer that stores recovered long-term representations in a form rapidly accessible to decision making. Under this framework, raw memory representations are assumed inaccessible or too distributed for decision making systems to act upon and instead require an intermediate term store or buffer for conscious access during choice or reasoning (Baddeley, 2000). Thus the PPC would act as a temporary buffer similar to those proposed to operate in verbal or visual working memory in order to make retrieved episodic memory contents rapidly available for ongoing reasoning or executive operations. Wagner et al. (2005) noted that each of these hypotheses accounts for different aspects of the data, that they may not be exclusive, and that different regions within the PPC may perform different functions (see also Naghavi & Nyberg, 2005).
A somewhat different perspective has arisen from the research of Cabeza, Ciaramelli, Olson, and Moscovitch (2008), who have proposed a close functional parallel between parietal activations during recognition, and those observed during research on visuo-spatial attention. Cabeza et al. (2008) connected work on the PPC and attention to the memory literature, emphasizing that that dorsal and ventral PPC regions are thought to have dissociable roles in visuo-spatial attention, such that the dorsal parietal cortex (DPC) appears more responsive to top-down attentional demands while the ventral parietal cortex (VPC) appears to be involved in bottom-up attentional capture. Turning to memory, this potentially explains why dorsal PPC regions show increased activation for low confidence memory judgments, when top down monitoring for diagnostic memory content is presumably maximal, whereas ventral parietal regions appear to demonstrate the greatest activation when recovered memory contents are presumably vivid and/or salient, for example, during recognition accompanied by contextual recollection. This framework had been dubbed the attention to memory model and asserts that dorsal parietal regions in the superior parietal lobule (SPL) are critical for the guided or top down search for episodic memory content, whereas ventral parietal regions in the inferior parietal lobule (IPL) are critical for the capture of attention when salient memory content is suddenly recovered.
In the current report we use a modified version of the Explicit Memory Cueing task developed by O'Connor, Han, and Dobbins (2010) to probe the functional significance of parietal responses during recognition judgment (for a blocked manipulation of recognition memory expectations see Herron, Henson, and Rugg (2004)). During the Explicit Memory Cueing task, anticipatory cues preceded each recognition memory probe indicating whether each upcoming memory item was likely to have been studied (“Likely Old”) or not (“Likely New”). One key finding of the report was that activation was highest in the lateral parietal region whenever the subjects' expectations were violated by the upcoming memoranda, regardless of whether these items were correctly judged old or new. This invalid memory cueing effect was present in left supramarginal gyrus and because it demonstrated that activation differed as a function of violated expectations for correctly judged new materials (viz., correct rejections), this led O'Connor et al. to reject the idea that lateral parietal cortex played a direct role in the successful recovery or storage of episodic information because such information should be largely absent during correct rejection of new materials (O'Connor et al., 2010).
Although the O'Connor et al. (2010) study linked lateral parietal responses with the violation of memorial expectations, there were several potential drawbacks to the design. First, uncued or neutral trials were not intermixed among the cued trials making it difficult to compare the cued responses to responses that should be analogous to those observed in standard recognition paradigms. Second, the validity of the cues was not explicitly provided to the subjects and was instead learned via feedback. Finally, both highly valid and random cues were used in different blocks in an attempt to examine carryover learning effects. These latter two manipulations likely added considerable individual variability in the extent to which participants consciously believed the cues to be predictive and generally lowered the power of the cues to drive decision biases. Here we eliminated these potentially problematic aspects by fully intermixing cued and uncued trials, and by explicitly and correctly informing subjects that all predictive cues were 75% accurate, and hence should be actively used to bolster recognition performance. As shown below, this procedure allowed us to isolate functionally distinct patterns of response in the left lateral parietal cortex, suggesting separate regions specialized for the orienting of attention following unexpectedly familiar vs. unexpectedly novel items. A third pattern was also present, similar to that identified in O'Connor et al. (2010) in which memory content that violated expectations (regardless of whether old or new) elicited increased activation.
Before turning to the procedure, we outline a putative model of memory orienting (Memory Orienting Model) and make a key distinction between functional interpretations of PPC that assume the region plays a direct causal role in accurate recognition (causal models) vs. interpretations that instead assume the region supports a functional role that is a consequence of recognition retrieval processes, but that does not directly support those retrieval processes (consequential models). The causal/consequential distinction is important because the two perspectives lead to divergent predictions about patterns of activations across conditions and about the link between brain activation and individual differences in recognition ability. For example, the episodic retrieval buffer model is a causal model. Under this framework, conscious access to episodic knowledge during reasoning and choice is directly mediated by and hence causally dependent upon PPC. Hence, an individual with a severely damaged episodic buffer cannot reliably evince accurate recognition and should be functionally amnesic. Furthermore, the level of activation of the buffer in a healthy individual should be a reliable index of the amount of episodic information currently available to decision making operations (Yu, Johnson, & Rugg, 2012). With all other things being equal, individuals who demonstrate a greater activation difference for studied vs. new items during testing should be more accurate because they are buffering more diagnostic episodic information in a form accessible to conscious recognition judgment. Overall, the episodic buffer, mnemonic accumulator, and VPC attentional capture component of the attention to memory model are all causal models. In each case, the function ascribed to the relevant portion of PPC is logically essential for, and indicative of, accurate recognition judgment.
Consequential models lead to a different set of predictions. Under these frameworks, activation in PPC, while dependent on retrieval processes, does not directly support those retrieval processes. Instead the activation represents a consequence that follows retrieval under certain contexts or task demands. The top down attention component of the attention to memory framework is potentially consistent with a consequential model. Under the model, Cabeza and colleagues assume that weak or ambiguous memory signals lead to the increased engagement of top down monitoring for memory content in SPL region(s). Such top down engagement would also presumably arise even without ambiguous signals, if instead the observers were simply forewarned that an upcoming recognition demand would be quite difficult. In terms of individual differences in recognition skill, observers who are highly skilled would presumably require engagement of this region less often than those who were unskilled because the latter would be much more likely to encounter ambiguous memory signals. Critically, if the monitoring operation did not noticeably improve or directly interact with retrieval processes, then the top down attention component of the attention to memory model would be consequential in that damage to the region would not lead to any gross impairment in basic recognition ability. Currently, however, the degree to which this component is thought to directly facilitate retrieval is somewhat unclear in the discussions of the model.
Based on the work of O'Connor et al. (2010) and the large literature linking PPC with visuo-spatial and other forms of attentional orienting we hypothesize that its role during recognition is also linked to orienting behavior. Thus PPC activation is a marker of the degree to which a memory signal is unexpected in a given context. As in other orienting domains, the primary purpose of this orienting response is investigatory. That is, the response is assumed to signal and eventually aid in the resolution of a perceived ambiguity. We discuss the evolutionary importance of resolving unexpected novelty and familiarity signals more in the discussion section, but here we note that the idea of memory orienting is not new among memory researchers. For example, in the dual process recognition theory of Mandler, item familiarity can play a key orienting role as exemplified by the oft-cited ‘Butcher-on-the-bus’ anecdote presented in that influential paper (Mandler, 1980). The anecdote describes a situation where upon boarding a bus, one's attention is captured by a fellow passenger who is oddly familiar, but whose familiarity initially defies explanation. Finally, following a deliberate source monitoring attempt involving several considered possible sources (e.g., is he from work?, the milkman?, etc.) one generates the appropriate cue and recollects that the individual is in fact the butcher from the local supermarket (for a more elaborate illustration see chapter 11 Baddeley, 1998).
This anecdote is not really one of recognition memory per se, but one highlighting how recognition signals can lead to an initial orienting response (the original attentional capture by the unexpectedly familiar passenger) and to subsequent deliberative attempts to explain the environmental ambiguity detected by the initial orienting response (deliberative memory search). Here the potentially more controlled retrieval behavior (source monitoring) is a consequence of an initial uncontrolled detection of an anomalous familiarity signal, but critically, neither the orienting response nor the deliberative attempts to explain that orienting response are causal with respect to the initial recognition process that begun the sequence. Thus, while the ability to discriminate the novel from the familiar is a prerequisite to the orienting phenomenon, it does not explain that phenomenon. More formally, recognition discrimination ability is necessary but not sufficient for the orienting phenomenon. The dependency of orienting on early discrimination ability is a characteristic of all orienting models. For example, in the Posner spatial cueing paradigm, small central arrows are used to forecast the spatial position of subsequent targets of either detection or discrimination (Posner & Petersen, 1990). These cues are generally valid and hence observers shift their covert spatial attention to the cued regions to facilitate or ease future judgments. Critically, when stimuli instead appear in the unexpected/uncued location it is assumed that parietal orienting mechanisms disengage attention from the expected region and drive attention towards the discrepancy. What is perhaps less appreciated, because the locations used are perfectly discriminable, is that this orienting mechanism necessarily depends on a core ability of the observer to discriminate between the left and right side of space in the absence of spatial cueing. Thus spatial orienting presumes spatial discrimination ability (which in the typical paradigm is presumably at ceiling for all subjects given the eccentricities typically used), and the observer's spatial discrimination ability will contribute to how salient violations of cued expectations are. Thus, we propose a Memory Orienting Model of PPC activation that is in line with these broad characteristics. Activation is presumed to reflect the degree to which initial recognition signals confirm vs. contradict expectations, and the ability of observers to discriminate the novel from the familiar in the absence of cues will contribute to the salience of the detected violations of expectation (and hence size of the orienting response) under cueing. The model is strictly consequential in that the PPC orienting responses are a reaction to initial unexpected recognition signals, but they do not causally contribute to the initial retrieval process itself. The adaptive function of the responses is to investigate and potentially resolve the perceived memory discrepancy, and as we demonstrate in the results, it appears that different mechanisms are recruited for orienting to unexpected novelty compared to orienting to unexpected familiarity in the environment.
Section snippets
Participants-main study
Eighteen individuals aged 19–35 years (8 female, mean age, 24.8; SD, 3.54) participated in the study. Written informed consent was obtained in accordance with the Institutional Review Board of Washington University in St. Louis. Two participants were excluded due to reporting nausea, and one due to falling asleep during scanning, leaving fifteen individuals for analysis. One of the fifteen participants failed to finish the final experimental block, but the completed blocks were included for
Behavior-analysis
Accuracy was initially considered using a mixed ANOVA with factors of Outcome (Hit vs. Correct Rejection – CR) and Cue Type (Likely Old – LO, Likely New – LN, or Uncued – UC). There was no main effect of Outcome (F<1) indicating that overall hits and correct rejection rates were similar. The main effect of Cue Type also failed to reach significance (F(2,28)=2.43, MSe=0.003, p=0.106) suggesting that the average correct response rates were similar across the three cueing conditions. Finally,
Discussion
The current study demonstrates considerable functional heterogeneity in the left lateral parietal cortex response during recognition judgment, and furthermore, that this heterogeneity is linked to the discordance between memory expectations and memory evidence. Three separate patterns were discovered. An unexpected familiarity response was observed in the anterior angular gyrus, which demonstrated greater activation for hits than correct rejections during the “Likely New” cue condition, when
Conclusion
In conclusion, the left lateral parietal cortex appears to support functionally distinct attentional orienting processes triggered by early episodic recognition signals. We view the role of these responses as investigatory processes that are triggered by recognition signals when they are discordant with expectations. Because the orienting is the consequence of discrepant recognition signals we refer to this Memory Orienting Model as consequential and not causal with respect to recognition
Acknowledgments
This research was supported by National Institutes of Health grant R01 NIMH073982 to I.G.D.
References (35)
- et al.
Parietal contributions to recollection: electrophysiological evidence from aging and patients with parietal lesions
Neuropsychologia
(2008) - et al.
Visual and oculomotor selection: links, causes and implications for spatial attention
Trends in Cognitive Sciences
(2006) The episodic buffer: a new component of working memory?
Trends in Cognitive Sciences
(2000)- et al.
Cognitive contributions of the ventral parietal cortex: an integrative theoretical account
Trends in Cognitive Sciences
(2012) - et al.
The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability
Neuroimage
(2006) - et al.
Does lateral parietal cortex support episodic memory? Evidence from focal lesion patients
Neuropsychologia
(2008) - et al.
Executive control during episodic retrieval: multiple prefrontal processes subserve source memory
Neuron
(2002) - et al.
Use of explicit memory cues following parietal lobe lesions
Neuropsychologia
(2012) - et al.
Memory orientation and success: separable neurocognitive components underlying episodic recognition
Neuropsychologia
(2003) - et al.
Probability effects on the neural correlates of retrieval success: an fMRI study
Neuroimage
(2004)
Common fronto-parietal activity in attention, memory, and consciousness: shared demands on integration?
Consciousness and Cognition
A parcellation scheme for human left lateral parietal cortex
Neuron
Parietal lobe contributions to episodic memory retrieval
Trends in Cognitive Science
Human memory: Theory and practice
The parietal cortex and episodic memory: an attentional account
Nature Reviews Neuroscience
Overlapping parietal activity in memory and perception: evidence for the attention to memory model
Journal of Cognitive Neuroscience
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These authors contributed equally to this project.