Anthony D. Wagner

Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex.

Neuroimaging and neuropsychological studies have implicated left inferior prefrontal cortex (LIPC) in both semantic and phonological processing. In this study, functional magnetic resonance imaging was used to examine whether separate LIPC regions participate in each of these types of processing. Performance of a semantic decision task resulted in extensive LIPC activation compared to a perceptual control task. Phonological processing of words and pseudowords in a syllable-counting task resulted in activation of the dorsal aspect of the left inferior frontal gyrus near the inferior frontal sulcus (BA 44/45) compared to a perceptual control task, with greater activation for nonwords compared to words. In a direct comparison of semantic and phonological tasks, semantic processing preferentially activated the ventral aspect of the left inferior frontal gyrus (BA 47/45). A review of the literature demonstrated a similar distinction between left prefrontal regions involved in semantic processing and phonological/lexical processing. The results suggest that a distinct region in the left inferior frontal cortex is involved in semantic processing, whereas other regions may subserve phonological processes engaged during both semantic and phonological tasks.

Parietal lobe contributions to episodic memory retrieval.

Although the parietal lobe is not traditionally thought to support declarative memory, recent event-related fMRI studies of episodic retrieval have consistently revealed a range of memory-related influences on activation in lateral posterior parietal cortex (PPC) and precuneus extending into posterior cingulate and retrosplenial cortex. This article surveys the fMRI literature on PPC activation during remembering, a literature that complements earlier electroencephalography data. We consider these recent memory-related fMRI responses within the context of classical ideas about parietal function that emphasize space-based attention and motor intention. We conclude by proposing three hypotheses concerning how parietal cortex might contribute to memory.

Recovering meaning: left prefrontal cortex guides controlled semantic retrieval.

Prefrontal cortex plays a central role in mnemonic control, with left inferior prefrontal cortex (LIPC) mediating control of semantic knowledge. One prominent theory posits that LIPC does not mediate semantic retrieval per se, but rather subserves the selection of task-relevant knowledge from amidst competing knowledge. The present event-related fMRI study provides evidence for an alternative hypothesis: LIPC guides controlled semantic retrieval irrespective of whether retrieval requires selection against competing representations. With selection demands held constant, LIPC activation increased with semantic retrieval demands and with the level of control required during retrieval. LIPC mediates a top-down bias signal that is recruited to the extent that the recovery of meaning demands controlled retrieval. Selection may reflect a specific instantiation of this mechanism.

Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories

A central function of memory is to permit an organism to distinguish between stimuli that have been previously encountered and those that are novel. Although the medial temporal lobe (which includes the hippocampus and surrounding perirhinal, parahippocampal, and entorhinal cortices) is known to be crucial for recognition memory, controversy remains regarding how the specific subregions within the medial temporal lobe contribute to recognition. We used event-related functional MRI to examine the relation between activation in distinct medial temporal lobe subregions during memory formation and the ability (i) to later recognize an item as previously encountered (item recognition) and (ii) to later recollect specific contextual details about the prior encounter (source recollection). Encoding activation in hippocampus and in posterior parahippocampal cortex predicted later source recollection, but was uncorrelated with item recognition. In contrast, encoding activation in perirhinal cortex predicted later item recognition, but not subsequent source recollection. These outcomes suggest that the subregions within the medial temporal lobe subserve distinct, but complementary, learning mechanisms.

Cognitive control in media multitaskers

Chronic media multitasking is quickly becoming ubiquitous, although processing multiple incoming streams of information is considered a challenge for human cognition. A series of experiments addressed whether there are systematic differences in information processing styles between chronically heavy and light media multitaskers. A trait media multitasking index was developed to identify groups of heavy and light media multitaskers. These two groups were then compared along established cognitive control dimensions. Results showed that heavy media multitaskers are more susceptible to interference from irrelevant environmental stimuli and from irrelevant representations in memory. This led to the surprising result that heavy media multitaskers performed worse on a test of task-switching ability, likely due to reduced ability to filter out interference from the irrelevant task set. These results demonstrate that media multitasking, a rapidly growing societal trend, is associated with a distinct approach to fundamental information processing.

Medial Temporal Lobe Activations in fMRI and PET Studies of Episodic Encoding and Retrieval

Early neuroimaging studies often failed to obtain evidence of medial temporal lobe (MTL) activation during episodic encoding or retrieval, but a growing number of studies using functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) have provided such evidence. We review data from fMRI studies that converge on the conclusion that posterior MTL is associated with episodic encoding; too few fMRI studies of retrieval have reported MTL activations to allow firm conclusions about their exact locations. We then turn to a recent meta‐analysis of PET studies (Lepage et al., Hippocampus 1998;8:313–322) that appears to contradict the fMRI encoding data. Based on their analysis of the rostrocaudal distribution of activations reported during episodic encoding or retrieval, Lepage et al. (1998) concluded that anterior MTL is strongly associated with episodic encoding, whereas posterior MTL is strongly associated with episodic retrieval. After considering the evidence reviewed by Lepage et al. (1998) along with additional studies, we conclude that PET studies of encoding reveal both anterior and posterior MTL activations. These observations indicate that the contradiction between fMRI and PET studies of encoding was more apparent than real. However, PET studies have reported anterior MTL encoding activations more frequently than have fMRI studies. We consider possible sources of these differences. Hippocampus 1999;9:7–24.

Observing the transformation of experience into memory

The ability to remember ones past depends on neural processing set in motion at the moment each event is experienced. Memory formation can be observed by segregating neural responses according to whether or not each event is recalled or recognized on a subsequent memory test. Subsequent memory analyses have been performed with various neural measures, including brain potentials extracted from intracranial and extracranial electroencephalographic recordings, and hemodynamic responses from functional magnetic resonance imaging. Neural responses can predict which events, and which aspects of those events, will be subsequently remembered or forgotten, thereby elucidating the neurocognitive processes that establish durable episodic memories.

Executive control during episodic retrieval: Multiple prefrontal processes subserve source memory

During recognition, one may sense items as familiar (item memory) and additionally recollect specific contextual details of the earlier encounters (source memory). Cognitive theory suggests that, unlike item memory, source memory requires controlled cue specification and monitoring processes. Functional imaging suggests that such processes may depend on left prefrontal cortex (PFC). However, the nature and possible anatomical segregation of these processes remains unknown. Using functional magnetic resonance imaging, we isolated distinct response patterns in left PFC during source memory consistent with semantic analysis/cue specification (anterior ventrolateral), recollective monitoring (posterior dorsolateral and frontopolar), and phonological maintenance/rehearsal (posterior ventrolateral). Importantly, cue specification and recollective monitoring responses were not seen during item memory and were unaffected by retrieval success, demonstrating that the mere attempt to recollect episodic detail engages multiple control processes with different left PFC substrates.

Lobular Patterns of Cerebellar Activation in Verbal Working-Memory and Finger-Tapping Tasks as Revealed by Functional MRI

The lobular distributions of functional activation of the cerebellum during verbal working-memory and finger movement tasks were investigated using functional magnetic resonance imaging (fMRI). Relative to a rest control, finger tapping of the right hand produced ipsilateral-increased activation in HIV/HV [Roman numeral designations based on Larsell’s (Larsell and Jansen, 1972) nomenclature] and HVI and weaker activation in HVIII that was stronger on the ipsilateral side. For a working-memory task, subjects were asked to remember six (high load) or one (low load) visually presented letters across a brief delay. To assess the motoric aspects of rehearsal in the absence of working memory, we asked the subjects to repeatedly read subvocally six or one letters at a rate that approximated the internally generated rehearsal of working memory (motoric rehearsal task). For both tasks, bilateral regions of the superior cerebellar hemispheres (left superior HVIIA and right HVI) and portions of posterior vermis (VI and superior VIIA) exhibited increased activation during high relative to low load conditions. In contrast, the right inferior cerebellar hemisphere (HVIIB) exhibited this load effect only during the working-memory task. We hypothesize that HVI and superior HVIIA activation represents input from the articulatory control system of working memory from the frontal lobes and that HVIIB activation is derived from the phonological store in temporal and parietal regions. From these inputs, the cerebellum could compute the discrepancy between actual and intended phonological rehearsal and use this information to update a feedforward command to the frontal lobes, thereby facilitating the phonological loop.

Functional-Neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory

Recognition decisions can be based on familiarity, the sense that an item was encountered previously (item memory), and on recollection, the conscious recovery of contextual information surrounding a previous encounter with the item (e.g., source memory). Recognition with recollection is thought to depend on multiple mechanisms, including prefrontal “control” processes that guide retrieval and recapitulation mechanisms that reactivate posterior neocortical representations that were present at encoding. However, uncertainty remains regarding the precise nature of prefrontal contributions to recollection and the selectivity of recapitulation to veridical recollection. The present event-related functional magnetic resonance imaging study sought to examine whether regions showing “old-new” effects support processes sensitive to recollection success or recollection attempt and whether recapitulation of neocortical representations emerge during veridical recollection as well as during false recognition (i.e., false alarms) or whether false recognition resembles familiarity-based responding. Results revealed that multiple left prefrontal cortical regions were engaged during attempts to recollect previous contextual (source) details, regardless of the nature of the to-be-recollected details and of source recollection outcome (successful vs unsuccessful). Recapitulation effects were observed in regions sensitive to the encoding task, suggesting that veridical recollection entails the reactivation of processes or representations present during encoding. Importantly, in contrast to leading models of recognition memory, false alarms also appeared to be based partially on recollection, as revealed through false recapitulation effects. Implications for neural and cognitive models of recognition are considered.