Yifat FaranIntroduction
This article is a commentary on the role of BA10 in episodic memory, as predicted by Ben Shalom and Bonneh's (2019) model of the narrow prefrontal cortex. It aimed to explore whether there is any existing literature on memory that supports a connection between BA10 and episodic memory, and if so, what form this connection might take.
Historical context
Many studies have emphasized the crucial role of the frontal lobes in episodic memory (e.g., Piolino et al., 2007; Coste et al., 2015; for a review, see Vakil, 2023). Based on lesion studies, Stuss and Alexander (2005) suggested that the frontal lobes are involved in multiple strategic processes. Similarly, Moscovitch (1992) suggested that the frontal lobes support the memory system by applying top-down processes, such as the implementation of strategy, organization, and conceptual elaborative encoding and retrieval. However, as Stuss and Alexander contended, the frontal lobe is not a homogenous structure and has to be considered in view of its component parts. The most efficient subdivision is based on histology and is defined by Brodmann areas. This article focused on the prefrontal pole, known as Brodmann area 10 (BA10). Studies have shown the involvement of BA10 in many cognitive tasks, including prospective memory (Burgess et al., 2007; Raskin et al., 2018), planning (Volle et al., 2011), analogy solving (Qiu et al., 2008), multitasking (Gilbert et al., 2007; Roca et al., 2011), and more (for a review, see Snow, 2016).
The current article examined the involvement of BA10 in episodic memory, specifically, the predictions made by Ben Shalom and Bonneh (2019) (i.e., that BA10 is involved in the integration of memory episodes) and by Ben Shalom (2009) (i.e., that medial BA10 is involved in the representation of memory episodes themselves).
On the anatomical level, BA10 shows anatomical connections with brain structures involved in episodic memory. Moayedi et al. (2015) found that BA10 can be divided into two sub-regions: the medial cluster and bilateral lateral clusters. The medial cluster is functionally connected to the bilateral and medial PFC, bilateral precuneus/posterior cingulate cortex, ipsilateral lateral occipital cortex, bilateral parahippocampal gyri, bilateral subgenual cingulate cortex, and bilateral middle temporal gyrus, which are mostly associated with the default mode network (DMN; e.g., Buckner and Krienen, 2013; Mak et al., 2017). The bilateral lateral clusters are connected to the bilateral supplementary motor area, ventrolateral premotor cortex, lateral parietal area, dorsolateral prefrontal cortex, and bilateral anterior insula, which are mostly associated with the central-executive network (CEN; Li et al., 2021). BA10 also shows functional connectivity during memory tasks. For instance, Fritch et al. (2021) found that BA10 was functionally connected to the posterior hippocampus, associated with retrieval, but not with the anterior hippocampus, associated with encoding. This functional connectivity was found during retrieval but not during encoding.
On the functional level, a growing body of substantial evidence supports the involvement of BA10 in episodic memory. Numerous studies have demonstrated the involvement of BA10 in episodic retrieval and, to a lesser extent, in episodic encoding. For example, Lepage et al. (2000) reviewed imaging studies that focused on episodic memory retrieval and found that many of them showed activation in BA10 (e.g., Schacter et al., 1996; Rugg et al., 1998). Since then, a growing body of evidence has supported the role of BA10 in the retrieval of episodic memory, and retrieval efforts. However, studies that focus on encoding found less activation in this region. For instance, Fletcher and Henson (2001) reviewed studies that used imaging to test brain activation during both encoding and retrieval and found that, while only 2 out of 23 studies showed activation in BA10 during encoding, 15 out of 25 studies showed activation in BA10 during retrieval. This region has therefore been labeled as part of the retrieval success network. In a review of research that tested activation in response to repetition, Kim (2017) found that BA10, as part of the retrieval success network, indeed showed increased activation due to repetition.
Similarly, Weymar et al. (2018) reported that repetition enhancement was found in the medial posterior parietal (precuneus/cuneus), lateral parietal cortex (angular gyrus), and left BA10. However, some findings were less consistent with the idea that BA10 is involved in the integration of memory episodes. For example, King et al. (2005) showed that increasing the diversity between the contexts of the events, such as giving each item a different context to make them more distinct, reduced the activation in BA10.
A recent synthesis
Two questions can thus be asked regarding the connection between BA10 and episodic memory. The first question pertains to why BA10 is more active during retrieval than encoding. The second question concerns the nature of the actual connection between BA10 and episodic memory.
Some answers to both questions might lie in a recent study by Bonasia et al. (2018). In this article, the authors tested brain activation during the encoding and retrieval of video clips. Participants saw video clips that were either similar to events people encounter in everyday life, that is, congruent video clips, or video clips that were very unusual and/or dissimilar to anything people encounter in day-to-day life, that is, incongruent video clips. In addition, the authors also used neutral video clips that were neither very similar nor dissimilar to everyday life. As expected, the participants recalled both congruent and incongruent video clips better than neutral ones, indicating that both congruency and incongruity can enhance memory. However, brain activation in medial BA10 during encoding and retrieval was modulated by congruency alone. In a parametric analysis, during encoding, medial BA10 was more activated with increasing congruency. It also showed more functional connectivity during encoding with increasing congruency. Importantly, during retrieval, medial BA10 also showed increased functional connectivity with the increasing congruence of the retrieved material. These findings are consistent with those of other studies that showed increased activation of BA10 during repetition (Kim, 2017; Weymar et al., 2018) and reduced activation when the context between encoding and retrieval was changed (King et al., 2005).
It thus appears that the answer to the first question, i.e., why is BA10 activated more during retrieval than during encoding?, might lie in the fact that studied items are rarely considered in terms of their level of congruency, rather, they are more commonly compared between retrieval and encoding. Thus, when the relevant factor is not the level of congruency but retrieval vs. encoding, retrieved items, which have already been encountered, are, on average, more congruent with prior context than encoded items, resulting in additional BA10 activation. In addition, regarding the second question, what does this synthesis mean for the connection between BA10 and episodic memory? According to Bonasia et al. (2018), the medial BA10 detects congruence between current experiences and prior knowledge before activating relevant prior knowledge to facilitate comprehension and enhance the integration of new event-specific information with prior knowledge.
Discussion
As noted by Bonasia et al. (2018), their synthesis is consistent with Van Kesteren et al.'s (2012) SLIMM model (schema-linked interactions between medial prefrontal and medial temporal regions), according to which event congruence would affect activity and connectivity across the brain during both encoding and retrieval: increased congruence between events and prior knowledge correlating with activity in the medial prefrontal cortex, and increased incongruence between events and prior knowledge correlating with activity in the medial temporal lobe.
More importantly, the connection between BA10 and episodic memory indicates that incoming memory episodes are not represented in medial BA10. Instead, what is represented in medial BA10 is prior knowledge that, when activated, helps the integration of incoming episodes into prior knowledge. Thus, while there is indeed a connection between BA10 and episodic memory, as the Ben Shalom and Bonneh (2019) model predicted, it is not as straightforward as incoming memory episodes represented in medial BA10.
Author contributions
The author confirms being the sole contributor of this work and has approved it for publication.
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Ben Shalom, D. (2009). The medial prefrontal cortex and integration in autism. Neuroscientist 15, 589–598. doi: 10.1177/1073858409336371
Ben Shalom, D., and Bonneh, Y. S. (2019). The medial prefrontal cortex and integration in ASD and typical cognition. Front. Hum. Neurosci. 13, 74. doi: 10.3389/fnhum.2019.00074
Bonasia, K., Sekeres, M. J., Gilboa, A., Grady, C. L., Winocur, G., and Moscovitch, M. (2018). Prior knowledge modulates the neural substrates of encoding and retrieving naturalistic events at short and long delays. Neurobiol. Learn. Mem. 153, 26–39. doi: 10.1016/j.nlm.2018.02.017
Buckner, R. L., and Krienen, F. M. (2013). The evolution of distributed association networks in the human brain. Trends Cogn. Sci. 17, 648–665. doi: 10.1016/j.tics.2013.09.017
Burgess, P. W., Dumontheil, I., Gilbert, S. J., Okuda, J., Schölvinck, M. L., and Simons, J. S. (2007). “On the role of rostral prefrontal cortex (area 10) in prospective memory”, in Prospective Memory: Cognitive, Neuroscience, Developmental, and Applied Perspectives, eds M. Kliegel, M. A. McDaniel, and G. O. Einstein (Mahwah: Erlbaum).
Coste, C., Navarro, B., Vallat-Azouvi, C., Brami, M., Azouvi, P., and Piolino, P. (2015). Disruption of temporally extended self-memory system following traumatic brain injury. Neuropsychologia 71, 133–145. doi: 10.1016/j.neuropsychologia.2015.03.014
Fletcher, P. C., and Henson, R. N. A. (2001). Frontal lobes and human memory: insights from functional neuroimaging. Brain 124, 849–881. doi: 10.1093/brain/124.5.849
Fritch, H. A., Spets, D. S., and Slotnick, S. D. (2021). Functional connectivity with the anterior and posterior hippocampus during spatial memory. Hippocampus 31, 658–668. doi: 10.1002/hipo.23283
Gilbert, S. J., Williamson, I. D., Dumontheil, I., Simons, J. S., Frith, C. D., and Burgess, P. W. (2007). Distinct regions of medial rostral prefrontal cortex supporting social and nonsocial functions. Soc. Cogn. Affect. Neurosci. 2, 217–226. doi: 10.1093/scan/nsm014
Kim, H. (2017). Brain regions that show repetition suppression and enhancement: a meta-analysis of 137 neuroimaging experiments. Hum. Brain Mapp. 38, 1894–1913. doi: 10.1002/hbm.23492
King, J. A., Hartley, T., Spiers, H. J., Maguire, E. A., and Burgess, N. (2005). Anterior prefrontal involvement in episodic retrieval reflects contextual interference. Neuroimage 28, 256–267. doi: 10.1016/j.neuroimage.2005.05.057
Lepage, M., Ghaffar, O., Nyberg, L., and Tulving, E. (2000). Prefrontal cortex and episodic memory retrieval mode. Proc. Natl. Acad. Sci. 97, 506–511. doi: 10.1073/pnas.97.1.506
Li, J., Liu, J., Zhong, Y., Wang, H., Yan, B., Zheng, K., et al. (2021). Causal interactions between the default mode network and central executive network in patients with major depression. Neuroscience 475, 93–102. doi: 10.1016/j.neuroscience.2021.08.033
Mak, L. E., Minuzzi, L., MacQueen, G., Hall, G., Kennedy, S. H., and Milev, R. (2017). The default mode network in healthy individuals: a systematic review and meta-analysis. Brain Connect. 7, 25–33. doi: 10.1089/brain.2016.0438
Moayedi, M., Salomons, T. V., Dunlop, K. A., Downar, J., and Davis, K. D. (2015). Connectivity-based parcellation of the human frontal polar cortex. Brain Struct. Funct. 220, 2603–2616. doi: 10.1007/s00429-014-0809-6
Moscovitch, M. (1992). Memory and working-with-memory: a component process model based on modules and central systems. J. Cogn. Neurosci. 4, 257–267. doi: 10.1162/jocn.1992.4.3.257
Piolino, P., Desgranges, B., Manning, L., North, P., Jokic, C., and Eustache, F. (2007). Autobiographical memory, the sense of recollection and executive functions after severe traumatic brain injury. Cortex 43, 176–195. doi: 10.1016/S0010-9452(08)70474-X
Qiu, J., Li, H., Chen, A., and Zhang, Q. (2008). The neural basis of analogical reasoning: An event-related potential study. Neuropsychologia 46, 3006–3013. doi: 10.1016/j.neuropsychologia.2008.06.008
Raskin, S. A., Williams, J., and Aiken, E. M. (2018). A review of prospective memory in individuals with acquired brain injury. Clin. Neuropsychol. 32, 891–921. doi: 10.1080/13854046.2018.1455898
Roca, M., Torralva, T., Gleichgerrcht, E., Woolgar, A., Thompson, R., Duncan, J., et al. (2011). The role of Area 10 (BA10) in human multitasking and in social cognition: a lesion study. Neuropsychologia 49, 3525–3531. doi: 10.1016/j.neuropsychologia.2011.09.003
Rugg, M. D., Fletcher, P. C., Allan, K., Frith, C. D., Frackowiak, R. S. J., and Dolan, R. J. (1998). Neural correlates of memory retrieval during recognition memory and cued recall. Neuroimage 8, 262–273. doi: 10.1006/nimg.1998.0363
Schacter, D. L., Alpert, N. M., Savage, C. R., Rauch, S. L., and Albert, M. S. (1996). Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. Proc. Natl. Acad. Sci. 93, 321–325. doi: 10.1073/pnas.93.1.321
Snow, P. J. (2016). The structural and functional organization of cognition. Front. Hum. Neurosci. 10, 501. doi: 10.3389/fnhum.2016.00501
Stuss, D. T., and Alexander, M. P. (2005). Does damage to the frontal lobes produce impairment in memory? Curr. Direct. Psychol. Sci. 14, 84–88. doi: 10.1111/j.0963-7214.2005.00340.x
Vakil, E. (2023). “The mnemonic consequences of moderate-to-severe traumatic brain injury,” in Handbook of Human Memory, eds M. Kahana and A. Wagner (Oxford: Oxford University Press).
Van Kesteren, M. T., Ruiter, D. J., Fernández, G., and Henson, R. N. (2012). How schema and novelty augment memory formation. Trends Neurosci. 35, 211–219. doi: 10.1016/j.tins.2012.02.001
Volle, E., Gonen-Yaacovi, G., de Lacy Costello, A., Gilbert, S. J., and Burgess, P. W. (2011). The role of rostral prefrontal cortex in prospective memory: a voxel-based lesion study. Neuropsychologia 49, 2185–2198. doi: 10.1016/j.neuropsychologia.2011.02.045
Keywords: Brodmann area 10, episodic memory, posterior hippocampus, knowledge integration, retrieval
Citation: Faran Y (2023) A comment on the connection between BA10 and episodic memory. Front. Behav. Neurosci. 17:1105168. doi: 10.3389/fnbeh.2023.1105168
Received: 23 November 2022; Accepted: 07 April 2023;
Published: 05 May 2023.
Edited by:
Yoram S. Bonneh, Bar-Ilan University, IsraelReviewed by:
Moti Salti, Ben-Gurion University of the Negev, IsraelCopyright © 2023 Faran. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Yifat Faran, eWZpJiN4MDAwNDA7cG9zdC5iZ3UuYWMuaWw=