Neal E. A. Kroll

Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity

Memory for past events can be based on recollection or on assessments of familiarity. These two forms of human memory have been studied extensively by philosophers and psychologists, but their neuroanatomical substrates are largely unknown. Here we examined the brain regions that are involved in these two forms of memory by studying patients with damage to different temporal lobe regions. Our results come from (i) structural covariance modeling of recall and recognition, (ii) introspective reports during recognition and (iii) analysis of receiver operating characteristics. In sum, we found that the regions disrupted in mild hypoxia, such as the hippocampus, are centrally involved in conscious recollection, whereas the surrounding temporal lobe supports familiarity-based memory discrimination.

Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data.

Previous studies using the process dissociation and the remember-know procedures led to conflicting conclusions regarding the effects of anterograde amnesia on recollection and familiarity. We argue that these apparent contradictions arose because different models were used to interpret the results and because differences in false-alarm rates between groups biased the estimates provided by those models. A reanalysis of those studies with a dual-process signal-detection model that incorporates response bias revealed that amnesia led to a pronounced reduction in recollection and smaller but consistent reduction in familiarity. To test the assumptions of the model and to further assess recognition deficits in amnesics, we examined receiver operating characteristics (ROCs) in amnesics and controls. The ROCs of the controls were curved and asymmetrical, whereas those of the amnesics were curved and symmetrical. The results supported the predictions of the model and indicated that amnesia was associated with deficits in both recollection and familiarity.

Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study.

The temporal lobe regions involved in memory retrieval were examined using fMRI. During an associative recognition test, participants made memory judgments about the study color of previously presented drawings of objects, and during item recognition tests they made old/new judgments about previously studied objects or new objects. Associative recognition compared with old item recognition led to activations in bilateral hippocampal and parahippocampal regions, as well as in the left middle occipital gyrus. Old item recognition compared with new item recognition led to activation in the left middle occipital gyrus and the left middle temporal gyrus, and relative deactivations in bilateral hippocampal regions. The results indicate that partially distinct temporal lobe regions are involved during recognition memory for item and associative information.

Selective impairment of reasoning about social exchange in a patient with bilateral limbic system damage

Social exchange is a pervasive feature of human social life. Models in evolutionary biology predict that for social exchange to evolve in a species, individuals must be able to detect cheaters (nonreciprocators). Previous research suggests that humans have a cognitive mechanism specialized for detecting cheaters. Here we provide neurological evidence indicating that social exchange reasoning can be selectively impaired while reasoning about other domains is left intact. The patient, R.M., had extensive bilateral limbic system damage, affecting orbitofrontal cortex, temporal pole, and amygdala. We compared his performance on two types of reasoning problem that were closely matched in form and equally difficult for control subjects: social contract rules (of the form, “If you take the benefit, then you must satisfy the requirement”) and precaution rules (of the form, “If you engage in hazardous activity X, then you must take precaution Y”). R.M. performed significantly worse in social contract reasoning than in precaution reasoning, when compared both with normal controls and with other brain-damaged subjects. This dissociation in reasoning performance provides evidence that reasoning about social exchange is a specialized and separable component of human social intelligence, and is consistent with other research indicating that the brain processes information about the social world differently from other types of information.

Theta synchronization during episodic retrieval: neural correlates of conscious awareness.

The neural correlates of conscious awareness during successful memory retrieval were examined. In a recognition test, subjects indicated whether they consciously recalled the event in which a word was earlier presented (Remembering), or whether they recognized it on the basis that it was familiar in the absence of recollection (Knowing). An early EEG synchronization in the theta band predicted knowing, and a later remembering. Moreover, early and late event-related potentials were also found to predict knowing and remembering, respectively. The results indicate that the temporal dynamics of theta synchronization are related to the particular conscious experiences associated with memory retrieval.

Recognition memory for faces: When familiarity supports associative recognition judgments

Recognition memory for single items can be dissociated from recognition memory for the associations between items. For example, recognition tests for single words produce curvilinear receiver operating characteristics (ROCs), but associative recognition tests for word pairs produce linear ROCs. These dissociations are consistent with dual-process theories of recognition and suggest that associative recognition relies on recollection but that item recognition relies on a combination of recollection and assessments of familiarity. In the present study, we examined associative recognition ROCs for facial stimuli by manipulating the central and external features, in order to determine whether linear ROCs would be observed for stimuli other than arbitrary word pairs. When the faces were presented upright, familiarity estimates were significantly above zero, and the associative ROCs were curvilinear, suggesting that familiarity contributed to associative judgments. However, presenting the faces upside down effectively eliminated the contribution of familiarity to associative recognition, and the ROCs were linear. The results suggest that familiarity can support associative recognition judgments, if the associated components are encoded as a coherent gestalt, as in upright faces.

Novelty assessment in the brain and long-term memory encoding

Recent positron emission tomography (PET) studies have identified neuronal components of widespread novelty-assessment networks in the brain. We propose that the efficacy of encoding on-line information into long-term memory depends on the novelty of the information as determined by these networks, and report a test of this “novelty/encoding” hypothesis. Subjects studied a list of words. Half of the words were “familiar” by virtue of their repeated presentation to the subjects before the study of the critical list; the other half were novel, in that they had not previously been encountered in the experiment. The results conformed to the prediction of the novelty/encoding hypothesis: accuracy of explicit (episodic) recognition was higher for novel than for familiar words.

Autonomic responses to shock-associated words in a nonattended message: a failure to replicate.

Names of cities were shock associated and then embedded in material presented to the nonattended channel in a dichotic listening and shadowing situation. Despite earlier claims of differential responding to city names in the absence of awareness, no such differential responding was found. A test for conditioning following the dichotic listening task found that the subjects had been conditioned. Postexperimental interviews found that the subjects were aware of the city-shock contingency and had expected to be shocked during the dichotic listening task. Comparisons are made with other studies of galvanic skin responses to unattended words.

Recall and recognition in mild hypoxia: using covariance structural modeling to test competing theories of explicit memory.

To test theories of explicit memory in amnesia, we examined the effect of hypoxia on memory performance in a group of 56 survivors of sudden cardiac arrest. Structural equation modeling revealed that a single-factor explanation of recall and recognition was insufficient to account for performance, thus contradicting single-process models of explicit memory. A dual-process model of recall in which two processes (e.g., declarative memory and controlled search) contribute to recall performance, whereas only one process (e.g., declarative memory) underlies recognition performance, also failed to explain the results adequately. In contrast, a dual-process model of recognition provided an acceptable account of the data. In this model, two processes--recollection and familiarity--underlie recognition memory, whereas only the recollection process contributes to free recall. The best-fitting model was one in which hypoxia and aging led to deficits in recollection, but left familiarity unaffected. Moreover, a controlled search process was correlated with recollection, but was not associated with familiarity or the severity of hypoxia. The results support models of explicit memory in which recollection depends on the hippocampus and frontal lobes, whereas familiarity-based recognition relies on other brain regions.

The contribution of recollection and familiarity to yes-no and forced-choice recognition tests in healthy subjects and amnesics

Recent reports suggest that some amnesic patients perform relatively normally on forced-choice recognition memory tests. Their preserved performance may reflect the fact that the test relies more heavily on assessments of familiarity, a process that is relatively preserved in these patients, than do other recognition tests such as yes-no tests, which may rely more on recollection. The current study examined recognition memory using yes-no and forced-choice procedures in control and amnesic patients in order to determine whether the two tasks differentially relied on recollection and familiarity, and whether the extent of the recognition memory deficit observed in amnesia was dependent upon the type of recognition test used to measure performance. Results using the remember-know procedure with healthy subjects showed that there were no substantial differences in recognition accuracy or in the contribution of recollection to these two tasks. Moreover, amnesic patients were not found to perform better on a forced-choice test than on a yes-no test, suggesting that familiarity contributed equally to these two types of recognition test.