Research reportEncoding and retrieval related cerebral activation in continuous verbal recognition
Introduction
Functional neuroimaging studies have demonstrated a network of medio-temporal, frontal and parietal areas that subserve explicit encoding and recognition of previously studied material [5], [10]. With regard to the medial temporal lobe and the frontal lobe, models of spatial differentiation between encoding and retrieval have been proposed [28], [32], [39], [44]. However, both conditions have primarily been investigated in separate studies with different subjects, tasks and technical applications. The development of event-related functional magnetic resonance imaging (fMRI) [4], [14] now provides the basis to investigate different trial types in a single experiment. In the present study we used event-related fMRI to directly compare intermixed encoding and recognition of identical stimuli presented in a continuous recognition task.
The continuous recognition task has been widely employed in event-related potential (ERP) studies and robust differential effects of novel and repeated items, in terms of an increased negativity after the first presentation and a more positive ERP-waveform after the repeated presentation of target items, have been reported [11], [12], [34], [35]. Intracranial ERP studies have provided evidence for generators of the novel/repeated effects in various brain regions [16], [17], [18], [19], [20], [41], [42].
In the present study, we included two repetitions of the target items, contradictory to standard continuous recognition tasks, where the target item is repeated only once. This enabled us to address the issue of neuronal activation related retrieval effort, which has been a topic of debate in functional imaging studies [6], [7], [37]. Under the hypothesis that the retrieval effort is greater at the first repetition compared to the second repetition, the differential activation between these two conditions can be attributed to retrieval effort, if the retrieval success is equivalent.
In summary, the aims of the present study were (1) to directly compare encoding of novel items to recognition in an intermixed task design, and (2) to compare the recognition at first and second repetition to assess effects of retrieval effort. The interpretation of the results was restricted to memory relevant brain regions, namely the medial temporal, the medial and inferior frontal lobes and the inferior lateral and medial parietal lobes.
Section snippets
Subjects
Seventeen volunteers (eight female, nine male; mean age 26.7 years, range 22–36 years) gave written informed consent and participated in the study. All subjects were native German speakers. Nobody was suffering from any psychiatric, neurological or medical disease or was taking any medication at the time of the study. None of the participants had experienced a complication at birth or a head trauma. All subjects were right-handed according to the Edinburgh Handedness Inventory [33]. The study
Behavioural data
The subjects identified a mean of 31.7 (S.D.=2.0) of 34 words correctly as novel. 31.6 (S.D.=1.9) of 34 words were correctly identified as repeated after the first repetition. 33.4 (S.D.=0.6) of 34 words were correctly recognised as repeated after the second repetition. Thus, a near perfect recognition success of novel and repeated words was achieved. The reaction time (mean of first and second button press) over all items and all subjects was longer at the first (1.87 s, S.D.=0.43) than at the
Discussion
The aim of this study was (1) to directly compare cerebral activation related to encoding of novel and recognition of repeated items in a single experiment and (2) to detect areas of differential activation with respect to different levels of retrieval effort. The discussion focuses on areas that have been described to be involved in memory and is subdivided with regard to these different cerebral regions.
Conclusion
The direct comparison of cerebral activation related to encoding of novel items and recognition of repeated items in an intermixed experimental design revealed evidence of spatial differentiation of these memory subfunctions in the medial temporal, frontal and parietal lobe. The left medial parahippocampal gyrus is more active during encoding than during recognition, which is in agreement with intracranial ERP findings and fMRI studies that have reported encoding, but not retrieval related
References (48)
- et al.
Functional-anatomic study of episodic retrieval. II. Selective averaging of event-related fMRI trials to test the retrieval success hypothesis
Neuroimage
(1998) - et al.
Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success
Neuroimage
(1998) - et al.
The functional neuroanatomy of episodic memory
Trends Neurosci.
(1997) ERPs during continuous recognition memory for words
Biol. Psychol.
(1990)- et al.
Event-related fMRI: characterizing differential responses
Neuroimage
(1998) - et al.
Hemispheric specialization in human dorsal frontal cortex and medial temporal lobe for verbal and nonverbal memory encoding
Neuron
(1998) - et al.
Neural correlates of episodic retrieval success
Neuroimage
(2000) The assessment and analysis of handedness: the Edinburgh Inventory
Neuropsychologia
(1971)- et al.
Event-related potentials and the recollection of low and high frequency words
Neuropsychologia
(1995) - et al.
Human medial temporal lobe potentials evoked in memory and language tasks
Electroencephalogr. Clin. Neurophysiol.
(1986)
In what way does the parietal ERP old/new effect index recollection?
Int. J. Psychophysiol.
Short-term and long-term verbal memory: a positron emission tomography study
Proc. Natl. Acad. Sci. USA
Bestimmung der Bildhaftigkeit (I), Konkretheit (C) und der Bedeutungshaltigkeit (m′) von 800 substantiven
Z. Exp. Angewandte Psychol.
Making memories: brain activity that predicts how well visual experience will be remembered
Science
Event-related fMRI and the hemodynamic response
Hum. Brain Mapp.
Functional neuroimaging studies of encoding, priming, and explicit memory retrieval
Proc. Natl. Acad. Sci. USA
Task-related and item-related brain processes of memory retrieval
Proc. Natl. Acad. Sci. USA
Real-time tracking of memory formation in the human rhinal cortex and hippocampus
Science
Cognitive event-related potential components during continuous recognition memory for pictures
Psychophysiology
Statistical parametric mapping and other analyses of functional imaging data
Age-related reductions in human recognition memory due to impaired encoding
Science
Verbal novelty detection within the human hippocampus proper
Proc. Natl. Acad. Sci. USA
Limbic ERPs predict verbal memory after left-sided hippocampectomy
Neuroreport
Evidence relating human verbal memory to hippocampal N-methyl-d-aspartate receptors
Proc. Natl. Acad. Sci. USA
Cited by (14)
A parietal memory network revealed by multiple MRI methods
2015, Trends in Cognitive SciencesCitation Excerpt :Although early neuroimaging studies focused on the medial temporal and frontal lobes, parietal cortex has consistently been linked to human memory processing [10,11]. Numerous studies have associated parietal cortex with retrieval-success effects (see Glossary) [12–15], but regions of parietal cortex also show differential activity for: (i) subsequently forgotten, relative to subsequently remembered, items during memory encoding [16,17]; (ii) intentional retrieval tasks relative to intentional encoding tasks [18]; (iii) items that have been encoded multiple times relative to items that are encoded for the first time [19,20]; (iv) false alarms (new items judged as old) relative to misses (old items judged to be new) [21]; (v) more confidently, relative to less confidently, retrieved items [6]; and (vi) items for which rich, relative to sparse, contextual information is accessible at retrieval [7,22]. Hypotheses have been forwarded to explain these different patterns of data (see [10,23] for reviews), but no single hypothesis can account for all of the patterns described above.
Cognitive neurophysiology: Beyond averaging
2007, NeuroImageThe functional neuroanatomy of autobiographical memory: A meta-analysis
2006, NeuropsychologiafMRI evidence of word frequency and strength effects during episodic memory encoding
2005, Cognitive Brain ResearchDistinct prefrontal cortex activity associated with item memory and source memory for visual shapes
2003, Cognitive Brain ResearchBrain activation for effort in human learning: A critical and systematic review of fMRI studies
2018, International Journal of Psychology and Psychological Therapy