A role of perirhinal cortex (PrC) in recognition memory for objects has been well established. Contributions of parahippocampal cortex (PhC) to this function, while documented, remain less well understood. Here, we used fMRI to examine whether the organization of item-based recognition memory signals across these two structures is shaped by object category, independent of any difference in representing episodic context. Guided by research suggesting that PhC plays a critical role in processing landmarks, we focused on three categories of (...) objects that differ from each other in their landmark suitability as confirmed with behavioral ratings (buildings > trees > aircraft). Participants made item-based recognition-memory decisions for novel and previously studied objects from these categories, which were matched in accuracy. Multi-voxel pattern classification revealed category-specific item-recognition memory signals along the long axis of PrC and PhC, with no sharp functional boundaries between these structures. Memory signals for buildings were observed in the mid to posterior extent of PhC, signals for trees in anterior to posterior segments of PhC, and signals for aircraft in mid to posterior aspects of PrC and the anterior extent of PhC. Notably, item-based memory signals for the category with highest landmark suitability ratings were observed only in those posterior segments of PhC that also allowed for classification of landmark suitability of objects when memory status was held constant. These findings provide new evidence in support of the notion that item-based memory signals for objects are not limited to PrC, and that the organization of these signals along the longitudinal axis that crosses PrC and PhC can be captured with reference to landmark suitability. (shrink)

An alternative to Aggleton & Brown's interpretation is presented suggesting that the perirhinal cortex and hippocampus mediate different attribute information, but use the same processes, supporting the idea of parallel processing based on attribute (visual object and spatial location) rather than process characteristics (item recognition and familiarity).

Three comments are made. The proposal that recollection and familiarity-based recognition take different thalamic routes does not fit recent experimental evidence, suggesting that mediodorsal thalamus acts in an integrative role with respect to prefrontal cortex. Second, the role of frontal cortex in episodic memory has been understated. Third, the role of the hippocampal axis is likely to be the computation and storage of ideothetic information.

Perirhinal cortex contributes to judgements about stimulus familiarity, but its role is far greater than this. Impairments on tasks that do not involve familiarity judgements attest to the fact that perirhinal cortex is involved in the greater role of knowing about objects, including, but not limited to, their relative familiarity.

Aggleton & Brown argue that the function of the hippocampus and perirhinal cortex can be dissociated along a spatial/nonspatial dimension. They further suggest that this division corresponds to a distinction between episodic and recognition memory. An analysis of the data, however, fails to support the underlying dissociation.

A hippocampal patient is described who shows preserved item recognition and simple recognition-based recollection but impaired recall and associative recognition. These data and other evidence suggest that contrary to Aggleton & Brown's target article, Papez circuit damage impairs only complex item-item-context recollection. A patient with perirhinal cortex damage and a delayed global memory deficit, apparently inconsistent with A&B's framework, is also described.

Aggleton & Brown suggest that whereas familiarity is computed in perirhinal cortex, the hippocampus contributes to recollection. This account raises issues about the definition of amnesia, clarifies confusion about dual-process models of recognition, and sits comfortably with accounts of hippocampal function from outside the amnesia literature. The model can – and should – be tested. Some preliminary data suggest that it may need changes.

By utilizing new information from both clinical and experimental (lesion, electrophysiological, and gene-activation) studies with animals, the anatomy underlying anterograde amnesia has been reformulated. The distinction between temporal lobe and diencephalic amnesia is of limited value in that a common feature of anterograde amnesia is damage to part of an comprising the hippocampus, the fornix, the mamillary bodies, and the anterior thalamic nuclei. This view, which can be traced back to Delay and Brion (1969), differs from other recent models in (...) placing critical importance on the efferents from the hippocampus via the fornix to the diencephalon. These are necessary for the encoding and, hence, the effective subsequent recall of episodic memory. An additional feature of this hippocampalanterior thalamic and the perirhinal–medial dorsal thalamic systems are compromised, leading to severe deficits in both recall and recognition. (shrink)

The process of urban landmark-based navigation has proven to be difficult to study in a rigorous fashion, primarily due to confounding variables and the problem of obtaining reliable data in real-world contexts. The development of high-resolution, immersive virtual reality technologies has opened exciting new possibilities for gathering data on human wayfinding that could not otherwise be readily obtained. We developed a research platform using a virtual environment and electroencephalography to better understand the neural processes associated with landmark (...) usage and recognition during urban navigation tasks. By adjusting the architectural parameters of different buildings in this virtual environment, we isolated and tested specific design features to determine whether or not they served as a target for landmarking. EEG theta band event-related synchronization/desynchronization over posterior scalp areas was evaluated at the time when participants observed each target building along a predetermined self-paced route. A multi-level linear model was used to investigate the effects of salient architectural features on posterior scalp areas. Our results support the conclusion that highly salient architectural features—those that contrast sharply with the surrounding environment—are more likely to attract visual attention, remain in short-term memory, and activate brain regions associated with wayfinding compared with non-salient buildings. After establishing this main aggregate effect, we evaluated specific salient architectural features and neural correlates of navigation processing. The buildings that most strongly associated extended gaze time, location recall accuracy, and changes in theta-band neural patterns with landmarking in our study were those that incorporated rotational twist designs and natural elements such as trees and gardens. Other building features, such as unusual façade patterns or building heights, were to a lesser extent also associated with landmarking. (shrink)

Aggleton & Brown propose that familiarity-based recognition depends on a perirhinal-medial dorsal thalamic system. However, connections between these structures are sparse or absent. In contrast, the perirhinal cortex is connected to midline/intralaminar nuclei. In a human, a lesion in this thalamic domain, sparing the medial dorsal nucleus, impaired familiarity-based recognition while sparing recollective-based recognition. It is thus more likely that the intralaminar/midline nuclei are involved in recognition.

Based on theoretical considerations of Aurell (1979) and Block (1995), we argue that object recognition awareness is distinct from purely sensory awareness and that the former is mediated by neuronal activities in areas that are separate and distinct from cortical sensory areas. We propose that two of the principal functions of neuronal activities in sensory cortex, which are to provide sensory awareness and to effect the computations that are necessary for object recognition, are dissociated. We provide examples of how this (...) dissociation might be achieved and argue that the components of the neuronal activities which carry the computations do not directly enter the awareness of the subject. The results of these computations are sparse representations (i.e., vector or distributed codes) which are activated by the presentation of particular sensory objects and are essentially engrams for the recognition of objects. These final representations occur in the highest order areas of sensory cortex; in the visual analyzer, the areas include the anterior part of the inferior temporal cortex and the perirhinal cortex. We propose, based on lesion and connectional data, that the two areas in which activities provide recognition awareness are the temporopolar cortex and the medial orbitofrontal cortex. Activities in the temporopolar cortex provide the recognition awareness of objects learned in the remote past (consolidated object recognition), and those in the medial orbitofrontal cortex provide the recognition awareness of objects learned in the recent past. The activation of the sparse representation for a particular sensory object in turn activates neurons in one or both of these regions of cortex, and it is the activities of these neurons that provide the awareness of recognition of the object in question. The neural circuitry involved in the activation of these representations is discussed. (shrink)

Aggleton & Brown (A&B) propose that the hippocampal-anterior thalamic and perirhinal-medial dorsal thalamic systems play independent roles in episodic memory, with the hippocampus supporting recollection-based memory and the perirhinal cortex, recognition memory. In this commentary we discuss whether there is experimental support for the A&B model from studies of long-term memory in semantic dementia.

It is a consensus that familiarity and recollection contribute to episodic recognition memory. However, it remains controversial whether familiarity and recollection are qualitatively distinct processes supported by different brain regions, or whether they reflect different strengths of the same process and share the same support. In this review, I discuss how adapting standard human recognition memory paradigms to rats, performing circumscribed brain lesions and using receiver operating characteristic methods contributed to solve this controversy. First, I describe the validation of the (...) animal ROC paradigms and report evidence that familiarity and recollection are distinct processes in intact rats. Second, I report results from rats with hippocampal dysfunction which confirm this finding and lead to the conclusion that the hippocampus supports recollection but not familiarity. Finally, I describe a recent study focusing on the medial entorhinal cortex that investigates the contribution of areas upstream of the hippocampus to recollection and familiarity. (shrink)

Humans can recollect past events in details and/or know that an object, person, or place has been encountered before. During the last two decades, there has been intense debate about how recollection and familiarity are organized in the brain. Here, we propose an integrative memory model which describes the distributed and interactive neurocognitive architecture of representations and operations underlying recollection and familiarity. In this architecture, the subjective experience of recollection and familiarity arises from the interaction between core systems and an (...) attribution system. By integrating principles from current theoretical views about memory functioning, we provide a testable framework to refine the prediction of deficient versus preserved mechanisms in memory-impaired populations. The case of Alzheimer's disease is considered as an example because it entails progressive lesions starting with limited damage to core systems before invading step-by-step most parts of the model-related network. We suggest a chronological scheme of cognitive impairments along the course of AD, where the inaugurating deficit would relate early neurodegeneration of the perirhinal/anterolateral entorhinal cortex to impaired familiarity for items that need to be discriminated as viewpoint-invariant conjunctive entities. The integrative memory model can guide future neuropsychological and neuroimaging studies aiming to understand how such a network allows humans to remember past events, to project into the future, and possibly also to share experiences. (shrink)

Prior knowledge structures (or schemas) confer multiple behavioral benefits. First, when we encounter information that fits with prior knowledge structures, this information is generally better learned and remembered. Second, prior knowledge can support prospective planning. In humans, memory enhancements related to prior knowledge have been suggested to be supported, in part, by computations in prefrontal and medial temporal lobe cortex. Moreover, animal studies further implicate a role for the hippocampus in schema-based facilitation and in the emergence of prospective planning signals (...) following new learning. To date, convergence across the schema-enhanced learning and memory literature may be constrained by the predominant use of hippocampally dependent spatial navigation paradigms in rodents, and non-spatial list-based learning paradigms in humans. Here, we targeted this missing link by examining the effects of prior knowledge on human navigational learning in a hippocampally dependent virtual navigation paradigm that closely relates to foundational studies in rodents. Outside the scanner, participants overlearned Old Paired Associates (OPA – item-location associations) in multiple spatial environments, and they subsequently learned New Paired Associates (NPA – new item-location associations) in the environments while undergoing fMRI. We hypothesized that greater OPA knowledge precision would positively affect NPA learning, and that the hippocampus would be instrumental in translating this new learning into prospective planning of navigational paths to NPA locations. Behavioral results revealed that OPA knowledge predicted one-shot learning of NPA locations, and neural results indicated that one-shot learning was predicted by the rapid emergence of performance-predictive prospective planning signals in hippocampus. Prospective memory relationships were not significant in parahippocampal cortex and were marginally dissociable from the primary hippocampal effect. Collectively, these results extend understanding of how schemas impact learning and performance, showing that the precision of prior spatial knowledge is important for future learning in humans, and that the hippocampus is involved in translating this knowledge into new goal-directed behaviors. (shrink)

Scientists have shown that many non‐human animals such as ants, dogs, or rats are very good at using smells to find their way through their environments. But are humans also capable of navigating through their environment based on olfactory cues? There is not much research on this topic, a gap that the present research seeks to bridge. We here provide one of the first empirical studies investigating the possibility of using olfactory cues as landmarks in human wayfinding. Forty subjects participated (...) in a piloting study to determine the olfactory material for the main experiment. Then, 24 subjects completed a wayfinding experiment with 12 odors as orientation cues. Our results are astonishing: Participants were rather good at what we call “odor‐based wayfinding.” This indicates that the ability of humans to use olfactory cues for navigation is often underestimated. We discuss two different cognitive explanations and rule out the idea that our results are just an instance of sequential learning. Rather, we argue that humans can enrich their cognitive map of the environment with olfactory landmarks and may use them for wayfinding. (shrink)

In several experimental conditions, neuronal excitation at the perirhinal cortex (PC) does not propagate to the entorhinal cortex (EC) due to a “wall” of inhibition, which may help to create functional coupling and un‐coupling of the PC and EC in the medial temporal lobe. However, little is known regarding the coupling control process. Herein, we propose that the deep layer of area 35 in the PC plays a pivotal role in opening the gate for coupling, thus allowing the activity (...) in the PC to propagate to the EC. Using voltage‐sensitive dye imaging for the brain slices of rodents, we show that a slowly inactivating potassium conductance in this area is essential to induce excitation overtaking the inhibitory control. This coupling between the distinct neural circuits persists for at least 1 h. We elucidate further implications of this network‐level plastic behavior and its mechanism. (shrink)

To assess the ability of the disconnected cerebral hemispheres to recognize images of the self, a split-brain patient was tested using morphed self-face images presented to one visual hemifield at a time while making “self/other” judgments. The performance of the right and left hemispheres of this patient as assessed by a signal detection method was not significantly different, though a measure of bias did reveal hemispheric differences. The right and left hemispheres of this patient independently and equally possessed the ability (...) to self-recognize, but only the right hemisphere could successfully recognize familiar others. This supports a modular concept of self-recognition and other-recognition, separately present in each cerebral hemisphere. (shrink)

The accurate recognition of emotion is important for interpersonal interaction and when navigating our social world. However not all facial displays reflect the emotional experience currently being felt by the expresser. Indeed faces express both genuine and posed displays of emotion. In this article, we summarise the importance of motion for the recognition of face identity before critically outlining the role of dynamic information in determining facial expressions and distinguishing between genuine and posed expressions of emotion. We propose that both (...) dynamic information and face familiarity may modulate our ability to determine whether an expression is genuine or not. Finally, we consider the shared role for dynamic information across different face recognition tasks and the wider impact of face familiarity on determining genuine from posed expressions during real-world interactions. (shrink)

We can understand viewed scenes and extract task-relevant information within a few hundred milliseconds. This process is generally supported by three cortical regions that show selectivity for scene images: parahippocampal place area (PPA), medial place area (MPA) and occipital place area (OPA). Prior studies have focused on the visual information each region is responsive to, usually within the context of recognition or navigation. Here, we move beyond these tasks to investigate gaze allocation during scene viewing. Eye movements rely (...) on a scene’s visual representation to direct saccades, and thus foveal vision. In particular, we focus on the contribution of OPA, which is i) located in occipito-parietal cortex, likely feeding information into parts of the dorsal pathway critical for eye movements, and ii) contains strong retinotopic representations of the contralateral visual field. Participants viewed scene images for 1034 ms while their eye movements were recorded. On half of the trials, a 500 ms train of five transcranial magnetic stimulation (TMS) pulses was applied to the participant’s cortex, starting at scene onset. TMS was applied to the right hemisphere over either OPA or the occipital face area (OFA), which also exhibits a contralateral visual field bias but shows selectivity for face stimuli. Participants generally made an overall left-to-right, top-to-bottom pattern of eye movements across all conditions. When TMS was applied to OPA, there was an increased saccade latency for eye movements toward the contralateral relative to the ipsilateral visual field after the final TMS pulse (400ms). Additionally, TMS to the OPA biased fixation positions away from the contralateral side of the scene compared to the control condition, while the OFA group showed no such effect. There was no effect on horizontal saccade amplitudes. These combined results suggest that OPA might serve to represent local scene information that can then be utilized by visuomotor control networks to guide gaze allocation in natural scenes. (shrink)

This commentary reviews recent evidence that some hippo- campal functions do not depend on perirhinal inputs and discusses how the multiple-process model of recognition may shed interpretive light on previous reports of DNMS reacquisition deficits in pretrained subjects with hippocampal damage. Suggestions are made for determining whether nonhuman subjects solve object-recognition tasks using recollective memory or familiarity judgments.

Optic neuropathies are conditions that cause disease to the optic nerve, and can result in loss of visual acuity and/or visual field defects. An improved understanding of how these conditions affect the entire visual system is warranted, to better predict and/or restore the visual loss. In this article, we review visually-driven functional magnetic resonance imaging (fMRI) studies of optic neuropathies, including glaucoma and optic neuritis (ON); we also discuss traumatic optic neuropathy (TON). Optic neuropathy-related vision loss results in fMRI deficit (...) within the visual cortex, and is often strongly correlated with clinical severity measures. Using predominantly flickering checkerboard stimuli, glaucoma studies indicated retinotopic-specific cortical alteration with more prominent deficits in advanced than in early glaucoma. Some glaucoma studies indicate a reorganized visual cortex. ON studies have indicated that the impacted cortical areas are briefly hyperactive. For ON, brain deficits are greater in the acute stages of the disease, followed by (near) normalization of responses of the LGN, visual cortex, and the dorsal visual stream, but not the ventral extrastriate cortex. Visually-driven fMRI is sensitive, at least in ON, in discriminating patients from controls, as well as the affected eye from the fellow eye within patients. The use of a greater variety of stimuli beyond checkerboards (e.g., visual motion and object recognition) in recent ON studies is encouraging, and needs to continue to disentangle the results in terms of change over time. Finally, visually-driven fMRI has not yet been applied in TON, although preliminary efforts suggest it may be feasible. Future fMRI studies of optic neuropathies should consider using more complex visual stimuli, and inter-regional analysis methods including functional connectivity. We suggest that a more systematic longitudinal comparison of optic neuropathies with advanced fMRI would provide improved diagnostic and prognostic information. (shrink)

Explanations of Capgras delusion and prosopagnosia typically incorporate a dual-route approach to facial recognition in which a deficit in overt or covert processing in one condition is mirror-reversed in the other. Despite this double dissociation, experiences of either patient-group are often reported in the same way – as lacking a sense of familiarity toward familiar faces. In this paper, deficits in the facial processing of these patients are compared to other facial recognition pathologies, and their experiential characteristics mapped onto the (...) dual-route model in order to provide a less ambiguous link between facial processing and experiential content. The paper concludes that the experiential states of Capgras delusion, prosopagnosia, and related facial pathologies are quite distinct, and that this descriptive distinctiveness finds explanatory equivalence at the level of anatomical and functional disruption within the face recognition system. The role of skin conductance response as a measure of ‘familiarity’ is also clarified. (shrink)

Individuals differ greatly in their ability to learn and navigate through environments. One potential source of this variation is “directional sense” or the ability to identify, maintain, and compare allocentric headings. Allocentric headings are facing directions that are fixed to the external environment, such as cardinal directions. Measures of the ability to identify and compare allocentric headings, using photographs of familiar environments, have shown significant individual and strategy differences; however, the neural basis of these differences is unclear. Forty-five college students, (...) who were highly familiar with a campus environment and ranged in self-reported sense-of-direction, underwent fMRI scans while they completed the Relative Heading task, in which they had to indicate the direction of a series of photographs of recognizable campus buildings (i.e., “target headings”) with respect to initial “orienting headings”. Large individual differences were found in accuracy and correct decision latencies, with gender, self-reported sense-of-direction, and familiarity with campus buildings all predicting task performance. Using linear mixed models, the directional relationships between headings and the experiment location also impacted performance. Structural scans revealed that lateral orbitofrontal and superior parietal volume were related to task accuracy and decision latency, respectively. Bilateral hippocampus and right presubiculum volume were related to self-reported sense-of-direction. Meanwhile, functional results revealed clusters within the superior parietal lobule, supramarginal gyrus, superior frontal gyrus, lateral orbitofrontal cortex, and caudate among others in which the intensity of activation matched the linear magnitude of the difference between the orienting and target headings. While the retrosplenial cortex and hippocampus have previously been implicated in the coding of allocentric headings, this work revealed that comparing those headings additionally involved frontal and parietal regions. These results provide insights into the neural bases of the variation within human orientation abilities, and ultimately, human navigation. (shrink)

Simulation process and mirroring mechanism appear to be necessary to the recognition of emotional facial expressions. Prefrontal areas were found to support this simulation mechanism. The present research analyzed the role of premotor area in processing emotional faces with different valence , considering both conscious and unconscious pathways. High-frequency rTMS stimulation was applied to prefrontal area to induce an activation response when overt and covert processing was implicated. Twenty-two subjects were asked to detect emotion/no emotion . Error rates and response (...) times were considered in response to the experimental conditions. ERs and RTs decreased in case of premotor brain activation, specifically in response to fear, for both conscious and unconscious condition. The present results highlight the role of the premotor system for facial expression processing, supporting the existence of two analogous mechanisms for conscious and unconscious condition. (shrink)