The Inferior Parietal Lobule and Recognition Memory: Expectancy Violation or Successful Retrieval?

Abstract

Functional neuroimaging studies of episodic recognition demonstrate an increased lateral parietal response for studied versus new materials, often termed a retrieval success effect. Using a novel memory analog of attentional cueing, we manipulated the correspondence between anticipated and actual recognition evidence by presenting valid or invalid anticipatory cues (e.g., "likely old") before recognition judgments. Although a superior parietal region demonstrated the retrieval success pattern, a larger inferior parietal lobule (IPL) region tracked the validity of the memory cueing (invalid cueing Ͼ valid cueing) and no retrieval success-sensitive lateral parietal region was insensitive to cueing. The invalid cueing response occurred even for correctly identified new items unlikely to trigger substantive episodic retrieval. Within the IPL, although supramarginal and angular gyrus (SMG; AG) regions both demonstrated invalid cueing amplitude elevations, each region differentially coupled with distinct cortical networks when unexpectedly old items were encountered; a connectivity pattern also observed at rest in the same subjects. These findings jointly suggest that the lateral parietal response during recognition does not signify the recovery of episodic content, but is a marker of the violation of memory expectations. A second independent dataset confirmed this interpretation by demonstrating that SMG activation tracked the decision biases of observers, not their accuracy, with increased activation for nondominant recognition judgments. The expectancy violation interpretation of the lateral parietal recognition response is consistent with the literature on visual search and oddball paradigms and suggests that damage to these regions should impair memory-linked orienting behavior and not retrieval per se.

Pupil dilation during recognition memory: Isolating unexpected recognition from judgment uncertainty

“…This conceptualization is consistent with various recognition models inspired by functional neuroimaging that assume a role for bottom-up attention in the processing of unexpected memorial content (Cabeza, Ciaramelli, Olson & Moscovitch, 2008;O'Connor, Han & Dobbins, 2010) and it is also consistent with a recent conceptualization of the pupil dilation response as signalling the surprise value of diagnostic information during economic decision-making (Preuschoff, 't Hart & Einhauser, 2011). This characterization of the recognition pupil response as reflecting an involuntary orienting process has to date neither been considered nor tested.…”

“…We collected pupillometry data during recognition using an Explicit Memory Cueing paradigm developed by O'Connor, Han & Dobbins (2010). In the cued phase of the paradigm, cues or 'hints' which are known to be 70% valid precede each recognition memory probe ('Likely Old' or 'Likely New').…”

“…Hence, one should see increased dilation during correct responses to both invalidly cued new materials and invalidly cued old materials because in both cases judgment uncertainty is heightened compared to the valid cue conditions, and thus the effort required to reach a correct conclusion will also increase. This is because invalid cueing for both old and new materials has been shown to adversely affect judgment accuracy, speed and confidence, given that it sets up a conflict between recovered memorial signals and expectations (Jaeger et al, 2012;Jaeger, Konkel, & Dobbins, 2013;Konkel, Selmeczy, & Dobbins, 2015;O'Connor et al, 2010;Selmeczy & Dobbins, 2012). Increased dilation for both invalid cue types would converge with demonstrations of increased dilation during Stroop (Laeng et al, 2011) and Simon conflict manipulations (Steenbergen & Band, 2013), and in turn would support the idea that the previously reported pupil old/new effect indeed reflected the amount of volitional effort expended, which just happens to be larger on average for old versus new recognition conclusions in standard, uncued recognition paradigms.…”

Question format shifts bias away from the emphasised response in tests of recognition memory

“…Egan, 1958;O'Connor, et al, 2010;Ratcliff, et al, 1992;Rhodes & Jacoby, 2007). We suggest that our counter-emphasis bias differs from cue-driven biases in that it establishes a decision goal against which retrieved memory evidence is evaluated, rather than contributing to the evidence itself.…”

Recognition Without Identification, Erroneous Familiarity, and Déjà Vu

“…Spreading functional network activation provides the opportunity for a more distributed set of nodes (eg, regions Q, L, and F), which may be located in areas distant from region X, to be responsible for experience A (as globus pallidus stimulation caused contralateral mesial temporal activation in the discussed Kovacs et al [11] article), with further consideration of the temporal dynamics of this spreading activation introducing another point at which activation may deviate from nonaberrant activation [18]. The functional network region in which activation is localized is important to consider in light of findings that the displacement of functional connectivity "seed" regions by millimeters, even within the same brain structure, can lead to the identification of vastly different networks or the identification of differing regions on the borders of the same functional network [19,20]. This is perhaps most salient when comparing activation and experiences resulting from artificial electrical stimulation in separate 6 but closely spaced regions and should be considered together with the previous two factors.…”