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Les arts de la mémoire et les images mentales

Alain Berthoz
John Scheid

How does the brain build memory-relevant paths?

Giorgia Committeri et Gaspare Galati

Texte intégral

Introduction to the issue

  • 1 Scheid, 2012.

1John Scheid’s book, À Rome sur les pas de Plutarque1, presents a fascinating interpretation of Plutarch’s text Roman Questions, in which the series of questions concerning different aspects of life in Ancient Rome are primarily likened to a walk linking various places within a restricted space. Each of the questions is associated with the historical meaning and the characteristics of the places themselves. Plutarch’s text is thus seen as an exercise of the “arts of memory”, used since antiquity for memorizing places, objects or even concepts.

  • 2 Of the path and the Questions.

2In this article, we offer a neuroscientific point of view of the process of creating such memory-relevant paths or routes. This is a complex mental construction that requires the co-operation of multiple cognitive processes, together with the underlying neural correlates. The complex experience we are talking about calls for a cognitive dissection. One obvious component of this experience is spatial navigation, that is, the ability to determine and maintain a trajectory towards a goal location, which is necessary to keep ourselves oriented within the surrounding space during walking. Memory2 is obviously also involved, but language must likewise be taken into account, especially its semantic components, given the importance of the links/connections among the parts (places and events/notions), neatly reported in John Scheid’s book as “connexions thématiques/topographiques”. These connections constitute the building blocks of the resulting path, which develop as “events” as the individual moves about within the environment and hears or reads about different notions (historical facts, habits, etc.), finally reaching a configuration that we could call a “meaningful” (memory-relevant) path. In this way, semantic links conveyed by language are transformed into semantic knowledge.

  • 3 Newcombe et al., 2013.

3A first consideration is that navigation, like memory, is an ancient system which has evolved to respond to basic behavioral needs common to most animal species, such as exploring the world while managing to come back “home”. It depends on the representation of the location of environmental features with respect to one another, and on the positioning of an oriented moving self within the landscape. Together with intra-object representations and processes relevant to tool making, inter-object representations and processes relevant for navigation represent the “two distinct sets of spatial skills” that evolved in humans3.

  • 4 Bartlett, 1932.
  • 5 That is, linking elements in separate blocks according to shared features.
  • 6 For example, Giulio Camillo’s Theatre.
  • 7 Yates, 1966; Carruthers, 1990.

4A second aspect to take into consideration concerns the dynamic nature of both processes: memory is not static but rather a (re)construction4, something which is (re)built in time just like a path, linking different aspects of the individual experience, just as a path links different visited places or points in space. This is clearly shown by one crucial property that helps memorization: serialization or sequencing. This property, together with chunking5, has been historically exploited in order to increase memory power. The famous “journey” or “mental walk” technique constructs a memory path through an imagined walk into different places or points in space, like rooms within a palace. Palaces and theatres6 have been used as memory-training devices since the Middle Ages through the Renaissance, and are part of the so-called “arts of memory”, in which space/place represents a powerful trigger to the recall of information (objects, concepts, etc.) associated with it7. As we will see, this is due to the fact that our memory systems are context-dependent: we are predisposed to learn and remember things in a spatial (and temporal) context, even when there is no significant connection between the “thing” to remember and the place where it is “located”.

A neuroscientific point of view

  • 8 Maguire et al., 2003.

5The above-described spatial memory techniques or strategies have more recently been found to underlie the superior memory of people placed at the highest levels of the World Memory Championships. These “mental athletes” were studied while encoding different types of material (numbers, faces, snowflakes) and their strategies and neural activity compared to people without exceptional memory abilities8. Indeed, the group with superior memory reported to use the method of loci and functional magnetic resonance images (fMRI) revealed the involvement of a discrete set of brain regions, including the medial superior parietal cortex (precuneus), the retrosplenial cortex (RSC), and structures in the medial temporal lobe (MTL), in particular the posterior hippocampus. These regions were involved in the learning process per se and not merely in the efficacy of encoding.

  • 9 Reviewed in Boccia et al., 2014.
  • 10 Maguire et al., 2006.

6Importantly, these regions belong to a core network of brain regions which have been repeatedly associated with navigational tasks and route learning9, and which also include the parahippocampal cortex (PHC), another region in the MTL. One of these regions, the posterior hippocampus, was found to be bigger in volume in people with a long navigational experience, like London taxi drivers, compared to subjects without navigational experience and to bus drivers, who undergo a similar visual experience of environmental cues and stimuli, but follow fixed routes, rather than recalling and manipulating cognitive maps of the environment10. In particular, the hippocampal volume positively correlated with the years of experience as taxi drivers.

  • 11 Sulpizio et al., 2016.

7Not only does the experience shape the brain (in this case structurally), but individual differences in performance are also reflected in neural differences within the relevant brain networks, at the level of the intrinsic brain architecture. This has been measured through fMRI by assessing the functional coupling of spontaneous fluctuations of neural activity across brain regions in the absence of any externally imposed task. For example, we recently demonstrated that good navigators show higher coupling between the posterior hippocampus and the RSC than do poor navigators11.

  • 12 Committeri et al., 2004; Galati et al., 2010, Bastin et al., 2013.
  • 13 Sulpizio et al., 2013, 2015, 2016.
  • 14 Often called landmarks in the navigational literature.

8In a series of fMRI studies we conducted in collaboration with Alain Berthoz by means of two paradigms, the Palace paradigm12 and the Room paradigm13, we repeatedly found that the precuneus, the RSC and the PHC were critically involved in a process that we called “environmental referencing”. Across studies and across tasks, these regions were selectively activated whenever stable objects or features of the environment14 were used as spatial reference frames for perception and memory requirements.

  • 15 Aguirre and D’Esposito, 1999.
  • 16 Ino et al., 2007.
  • 17 For example, Habib and Sirigu, 1987.

9These are examples of what we learnt by studying healthy subjects with recent imaging techniques, but pathology had well before revealed the necessary role of the cited brain regions for efficient topographical perception, memory and orientation. Lesions to the lingual and parahippocampal gyri cause landmark agnosia, a difficulty in recognizing visual stimuli, which is selective for objects with an orienting value. Retrosplenial lesions, on the other hand, cause “heading disorientation”, a difficulty in deriving directional information from correctly recognized landmarks15 and, in some cases, in describing routes through correctly drawn maps of familiar places16. Finally, lesions to the hippocampal formation are followed by topographical amnesia, in which patients show memory loss in the cognitive representation of familiar or new environments17.

  • 18 Iaria et al., 2009.
  • 19 Iaria et al., 2014.
  • 20 Filippi and Agosta, 2011.
  • 21 Lim et al., 2010.
  • 22 Lim et al., 2010.

10More recently, a developmental form of topographical disorientation has been described18, in which the deficit is found in the absence of any structural lesion and with intact sensory and intellectual function. A lack of activation in the hippocampal complex and the retrosplenial cortex is evident in these patients when they are forming a cognitive map of a new environment, along with the breakdown of large-scale hippocampal functional connectivity, especially with the frontal lobe19. The breakdown of hippocampal connectivity is also evident in dementia such as in Alzheimer’s disease20 and in pre-clinical stages like mild cognitive impairment (MCI)21. Importantly, memory deficits are almost always the first symptoms to appear and are often accompanied by episodes of topographical disorientation that, when present, match with lesser functional abilities22.

11Taken together, the reported behavioral, neuroimaging and neuropsychological data demonstrate a strict link between memory performance and topographical orientation. This helps us to understand why and how spatial paths/routes can become so relevant for our memory.

Relevant neurocognitive models

  • 23 Kravitz et al., 2011.
  • 24 The so-called “parietal window” (Byrne et al., 2007).
  • 25 Boccia et al., 2016.

12From what we have seen until here, there is a dedicated brain network for navigation and orientation in environmental/topographical space. A recent review on visuospatial cognition refers to this network as the parieto-medial temporal stream of visual processing, parallel to and independent from the two well-known dorsal and ventral streams23. Within this network, the hippocampus and MTL regions are believed to be related to stable, environment-referenced, long-term spatial representations, as seen above, while parietal structures seemingly hold a temporary, detailed, and consciously accessible “live”, ego-referenced representation of our immediate surroundings, which is dynamically updated during navigation24. If that were so, the RSC would have a special role in “converting” long-term allocentric information to the parietal egocentric format, and vice versa. New types of human connectivity data show that the human hippocampus is indeed connected to the inferior parietal lobule (angular gyrus, AG) both directly and indirectly through the RSC25.

  • 26 Kravitz et al., 2011.

13Moreover, connections of the parietal cortex with prefrontal circuits26 subtend spatial working memory, i.e., the mechanism for temporarily maintaining spatial information in memory while processing and manipulating it. The role of the frontal cortex should also be noted with reference to other higher-level cognitive processes such as attentional control, motivation and emotion/affect, all involved when we experience and create the new associations that finally constitute what we have called above a “meaningful” path.

  • 27 Ritchley et al., 2015.
  • 28 Regions collectively described as the “default mode network” (Raichle et al., 2001).

14A neurocognitive model well suited to represent the complexity of such construction has recently been proposed as a general framework for memory27. This model, called the PMAT framework, is based on an extensive body of literature documenting differences in anatomical and functional connectivity among MTL structures. Within this model, the posterior-medial (PM) system includes several regions of the above-reported parieto-medial temporal visuospatial stream specialized for navigation (PHC, RSC, precuneus). In addition to scene perception and integration of one’s position within a global spatial context, it is linked to memory for the spatio-temporal context of an event, critical for the long-term storage of episodic and autobiographical memory. This is believed to be implemented through the connections of the PHC and the RSC with the posterior and anterior cingulate, the angular gyrus, and the ventromedial prefrontal cortex28. The anterior temporal (AT) system, on the other hand, includes regions like the perirhinal cortex (PRC) and the temporo-polar and lateral orbitofrontal cortex, which are believed to be involved in processing item/object information and long-term storage of previously learned items in the form of concepts. Therefore, in addition to object perception, this system is devoted to recognition and associative memory, as well as to semantic processing. Regions in the AT system are involved in processing and storing information about items/objects, including their perceptual and semantic features, as well as their salience and value.

15Importantly for the present context, both the PM and the AT system are heavily interconnected with the hippocampal formation. The connections are organized into two parallel streams at the level of both the entorhinal cortex (the PHC and the RSC primarily target the medial entorhinal cortex, while the PRC primarily targets the lateral entorhinal cortex) and the hippocampal subfields (the PHC shows preferential connectivity with the posterior part of the CA1 field, whereas the PRC shows preferential connectivity with the anterior part of the CA1 field). Both converging into the hippocampus, the two cortico-hippocampal systems work in strong functional interdependency, supporting memory-guided behavior by binding places and objects into events, and by creating semantic associations and therefore what we have called memory-relevant, meaningful paths.

Physical – neural coupling

16But what is the critical spatial information coded in these circuits, and how is it encoded in neuronal populations? The critical spatial quantities that must be encoded to support spatial orientation and navigation include at least our current location (where we are), the direction we are facing (what/where we are looking at), and where we are heading (the general orientation). These quantities need to be represented in relation to an externally defined frame, and also updated during our navigation. Recent human studies have started to shed light on how the MTL and related structures encode them.

  • 29 Sulpizio et al., 2014.

17We recently used the Room paradigm in conjunction with fMRI in order to systematically manipulate these quantities by exposing subjects to a random sequence of static views of a familiar immersive virtual world29. Neurophysiological signals from the hippocampal-parahippocampal-retrosplenial-parietal network described above were clearly modulated by the manipulation of these quantities, although in different ways. In the MTL, we found evidence for more stable and long-term coding of spatial locations and directions, with recognizable neural “signatures” associated to each individual location and direction within the room. In other words, the multivariate distribution of neural activity across different loci in the MTL allowed supra-chance decoding of the subject’s experienced location, direction they were facing, and direction they were heading, on the basis of neural signals. These “signatures” associated with each location and direction were independent of the specific recent “history” of experienced places and views. On the other hand, patterns of activity in the parietal lobe showed no systematic associations with individual locations and directions, but strong effects of the recent “history”: parietal activity decreased when experiencing more than once in a row the same location, facing direction, or heading (a phenomenon known as neural adaptation).

  • 30 Marchette et al., 2014.

18Interestingly, in this study the RSC exhibited both the MTL-like and the parietal-like effects, compatible with its role as a “hub” connecting allocentric MTL and egocentric parietal representations. Similar results were found by another study, where fixed environmental features (landmarks) were shown to be the anchor for the neural coding of location and facing direction of imagined viewpoints within the RSC30. Such results suggest that the RSC anchors internal spatial representations to local topographical features, thus allowing us to keep our orientation while navigating, and to retrieve from memory the experience of being in a particular place.

  • 31 Sulpizio et al., 2014.
  • 32 Sulpizio et al., 2017, 2018.

19Our study31 also allows some speculation about how patterns of neural activity encoding different locations are associated with each other to form a complex representation of the familiar environment. There has been much debate over the degree to which (or whether at all) we form long-term “maps” of the surrounding space. An interesting aspect of our results was that similarities between MTL activity patterns associated with different locations in the virtual world scaled with physical distances between the same locations: places and facing directions closer in physical space (in terms of physical distances) entailed activity patterns which were more similar (in terms of the global multivariate distance between the neural activity distributions). This is a form of “implicit” or distributed map: single locations need not be represented in separate populations of neurons, but may share the same neural population. Preliminary evidence from our laboratory shows that this finding can be partially generalized to larger environments32. What we suggest, therefore, is a form of coupling between space in the physical world and an abstract neuronal representational space constituted by the collective pattern of firing of hippocampal/MTL neurons.

  • 33 Campanile et al., 2018.
  • 34 Jadhav and Frank, 2014.

20This spatial physical/neural coupling brings us directly to a correspondence that is much older in time, and linked to evolutionary mechanisms. Buzsaki and Moser (2013) posited that memory mechanisms have evolved from mechanisms of navigation in the physical world. More specifically, the evolutionary roots of episodic and semantic memory systems are believed to be the path-integration (self-referenced, egocentric) and landmark-based (map-based, allocentric) forms of navigation, respectively. These two forms always work together, but the availability of external landmarks may determine whether one predominates over the other. Landmark-based navigation probably dominates in the case we are discussing, given the distributed reference to landmarks (e.g., the Capitolium and the Forum romanum) throughout the entire book. An environmental map is constructed by exploration and, similarly, semantic knowledge can be acquired through multiple personally experienced episodes with common elements. The mechanisms for representing a path through an environment are therefore similar to those used to represent sequences in memory. During physical travel, successive assemblies of neurons respond sequentially to the changing constellation of environmental landmarks and/or proprioceptive information from the body. By contrast, during mental travel, sequential activation is believed to be supported by self-organized patterning. Neuronal algorithms underlying navigation in real space and in mental space (memory) would thus be fundamentally the same: specific patterns and oscillatory dynamics in the entorhinal cortex and hippocampus, able to support both navigation and memory. Interestingly, recent preliminary data from our laboratory showed that participants with a better path integration ability, measured through a pure proprioceptive task, have a better episodic memory33. Moreover, during sleep or during quiet wakefulness following a waking experience in which a sequence has occurred (such as a session of maze exploration in rats or a route learning experience in humans), one can observe a reactivation or neuronal “replay” of hippocampal cells firing in a particular sequence34. This replay mechanism appears to be a fundamental mechanism needed to consolidate memory traces.


21The neuroscientific data and models presented here help us to understand why and how the sequential linking of spatial information encountered during a route, with non-spatial information to be remembered, is such a powerful mnestic tool. Only the efficient combined work of different large-scale neural systems processing memory and navigation, along with affect and motivation, can allow the complex and powerful mental “building” of meaningful semantic paths. Regarding the book by John Scheid, it is possible to speculate that the traveler/reader learnt something about Roman life (semantic memory) while living an intense personal experience through space (episodic memory), thus binding spatial information on places and views with different kinds of notions, through ancient mechanisms and systems that evolved in a strictly interrelated manner.


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1 Scheid, 2012.

2 Of the path and the Questions.

3 Newcombe et al., 2013.

4 Bartlett, 1932.

5 That is, linking elements in separate blocks according to shared features.

6 For example, Giulio Camillo’s Theatre.

7 Yates, 1966; Carruthers, 1990.

8 Maguire et al., 2003.

9 Reviewed in Boccia et al., 2014.

10 Maguire et al., 2006.

11 Sulpizio et al., 2016.

12 Committeri et al., 2004; Galati et al., 2010, Bastin et al., 2013.

13 Sulpizio et al., 2013, 2015, 2016.

14 Often called landmarks in the navigational literature.

15 Aguirre and D’Esposito, 1999.

16 Ino et al., 2007.

17 For example, Habib and Sirigu, 1987.

18 Iaria et al., 2009.

19 Iaria et al., 2014.

20 Filippi and Agosta, 2011.

21 Lim et al., 2010.

22 Lim et al., 2010.

23 Kravitz et al., 2011.

24 The so-called “parietal window” (Byrne et al., 2007).

25 Boccia et al., 2016.

26 Kravitz et al., 2011.

27 Ritchley et al., 2015.

28 Regions collectively described as the “default mode network” (Raichle et al., 2001).

29 Sulpizio et al., 2014.

30 Marchette et al., 2014.

31 Sulpizio et al., 2014.

32 Sulpizio et al., 2017, 2018.

33 Campanile et al., 2018.

34 Jadhav and Frank, 2014.


Laboratory of Neuropsychology and Cognitive Neuroscience, Department of Neuroscience, Imaging and Clinical Sciences, and Institute for Advanced Biomedical Technologies (ITAB), University G. d’Annunzio, Chieti, Italy
Brain Imaging Laboratory, Department of Psychology, Sapienza University, and Cognitive and Motor Rehabilitation and Neuroimaging Unit, Santa Lucia Foundation, Rome, Italy

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