Hemispheric asymmetries of memory: the HERA model revisited

Abstract

The hemispheric encoding/retrieval asymmetry (HERA) model is a process-specific description of experimental data provided by a large set of functional neuroimaging studies. According to HERA, left prefrontal cortex (PFC) is more involved than right PFC in episodic memory encoding, whereas right PFC is more involved than left PFC in episodic memory retrieval. Recently it has been claimed that this description does not hold for nonverbal materials. Here we propose a more precise formulation of HERA than previously, and argue that there is sufficient evidence to conclude that HERA, as reformulated, is true for both verbal and non-verbal materials.It has been known for some time now that structures within the two cerebral hemispheres do not contribute equally to mental activity [1]. The best known form of such hemispheric asymmetry is language: the left hemisphere is more involved in verbal processing than is the right. A more recent addition to the list of hemispheric asymmetries, although limited to the frontal regions of the brain, emerged from early PET studies of memory, and had to do with component processes of memory. Data from numerous studies showed that during learning of new material (encoding), left PFC tended to be more active than right PFC, whereas during a subsequent recall or recognition test (retrieval), right PFC tended to be more active than left PFC. This general pattern of data, initially based only on a handful of studies [2,3], was dubbed the Hemispheric Encoding/Retrieval Asymmetry (HERA) model. Figure 1 illustrates the HERA asymmetry with data from a single study.Although exceptions to HERA have been reported, numerous PET and fMRI studies have confirmed the existence of the general HERA pattern (for reviews see [4 -7]). Recently, however, it has been suggested [8][9][10][11][12][13][14] that the asymmetry of PFC activations might reflect the nature of the materials involved in the comparison tasks (verbal versus non-verbal) rather than the memory processes (encoding versus retrieval). In light of these recent challenges, it is timely to re-evaluate the situation. We propose a more precise formulation of HERA, and argue that the challenges to it are based on confusion about what HERA is, and about what kinds of data are, and are not, relevant to it. HERA revisedThe confusion is partly attributable to the looseness of the early formulation of HERA, and partly to subtleties of the relations involved. Here, in keeping with similar suggestions [10,15], we propose a stricter formulation of HERA. We suggest that the neuroanatomical data relevant to HERA should be based on a direct comparison of the two processes involved, with other variables, including materials, held constant.Let us abbreviate encoding as Enc, retrieval as Ret, a given site in left PFC as L, and the corresponding site in right PFC as R. And let us use the combination of tasks (Enc or Ret) and sites (L or R) to represent the level of (indirectly) measured neuronal activity at a given site in a given task.Then the encoding compon...

Prefrontal contributions to domain-general executive control processes during temporal context retrieval

“…In addition, activity in right DLPFC was significantly correlated with recency accuracy, and marginally correlated with recency RT. In general, our findings of greater right DLPFC activity during retrieval events versus ordering events are consistent with studies that have found greater right PFC during EM retrieval in general (Habib, Nyberg, & Tulving, 2003;Nyberg, Cabeza, & Tulving, 1996) and during temporal context retrieval specifically (Dobbins, Rice, Wagner, & Schacter, 2003;Konishi et al, 2002;Rajah & McIntosh, 2006;Suzuki et al, 2002). However, due to the relatively short delay (30 sec) between encoding and retrieval in the current study design, it may be argued that the retrieval tasks employed in this study reflected retrieval from WM and not from EM.…”

Human cortical EEG rhythms during long-term episodic memory task. A high-resolution EEG study of the HERA model

“…These results agreed with the so-called hemispherical encoding retrieval asymmetry (HERA) theory on the functional inter-hemispherical asymmetry during the long-term memorization of episodes (Lepage et al, 2000;Nyberg et al, 1996;Tulving et al, 1994). This model is now the focus of a lively discussion based on an increasing number of imaging studies that have attempted to characterize other factors affecting both the hemispheric asymmetry and the functional neuroanatomical subdivisions of frontal activation (Habib et al, 2003). It should be remarked that a HERA pattern is not an absolute feature of cortical activity during long-term memorization.…”

“…The ENC condition induced a stronger gamma ERS in left than right parietal area, while the RET condition showed a prominent gamma ERS in right compared to left parietal area. This hemispheric asymmetry did not regard the frontal responses and, therefore, seems to be inconsistent with the classical formulation of the HERA predictions, which is based on the function of the prefrontal areas (Habib et al, 2003). Furthermore, an evident right frontal gamma ERS was observed in RET condition but not in ENC condition.…”

“…Furthermore, for ENC condition, the ERS peak was stronger in left than right parietal areas ( P < 0.04), while, for RET condition, ERS peak was stronger in right than left frontal areas ( P < 0.008) and in right than left parietal areas ( P < 0.005). These results thus indicate the presence of an asymmetry in agreement with the HERA model in its most recent and stringent formulation (Habib et al, 2003), which however involves the parietal, rather than the prefrontal areas. Of note, a control ANOVA design for each band of interest demonstrated that the above findings were not due to a different baseline band power.…”

Memory Retrieval in Mice and Men

“…Different regions of the PFC have been implicated in mnemonic processes that support retrieval, particularly in domaingeneral processes, such as setting the retrieval mode or orientation, initiating the retrieval attempt, monitoring, goal-directed manipulation of retrieved information and overcoming of interference (Shimamura 1995;Rugg et al 1996;Moscovitch and Winocur 2002;Badre and Wagner 2007;Blumenfeld and Ranganath 2007). Several functional divisions of the PFC have been suggested, from the original hemispheric encoding/retrieval asymmetry (HERA) model that proposed preferential right PFC involvement in retrieval (Tulving et al 1994;Habib et al 2003;see Cabeza et al 2003 for an alternate hypothesis regarding the roles of left/ right PFC in retrieval), to within-hemispheric divisions according to medial/lateral, anterior/ posterior and dorsal/ventral axes attributing specific mnemonic processes to each subregion (Fletcher and Henson 2001;Wagner et al 2001;Petrides 2002;Simons et al 2005;Badre and Wagner 2007).…”