Familiarity impairments after anterior temporal-lobe resection with hippocampal sparing: Lessons learned from case NB

Abstract

We review evidence from an extensive single case study in an individual (NB) who underwent a rare left-sided anterior temporal-lobe resection with sparing of the hippocampus. Our study aimed to determine whether memory functions of perirhinal cortex, which was largely removed in the resection, can be impaired against a background of preserved hippocampus-dependent memory processing. This research was guided by the proposal that item-based familiarity assessment relies on contributions of perirhinal cortex, and that the hippocampus plays a unique role in the relational binding of items to episodic contexts, which is critical for recollection. Seven sets of findings have emerged from this research in NB and from follow-up work in other patients: (i) Familiarity impairments can be selective and be revealed with multiple methods; (ii) selective familiarity and selective recollection impairments can be double dissociated; (iii) selective familiarity impairments show material specificity; (iv) selective familiarity impairments extend to assessment of cumulative lifetime experience; (v) selective familiarity impairments are sensitive to degree of feature overlap between object concepts; (vi) selective familiarity impairments are associated with preserved task-related fMRI signals in the hippocampus; (vii) selective familiarity impairments can be observed in other lesion cases. Despite our main focus on the dual-process framework, we also discuss implications for the functional organization of the medial temporal lobes in broader terms. We argue that our findings shed light on this organization even if the functional specialization of different medial temporal structures is ultimately not fully captured with reference to the cognitive distinction between familiarity and recollection.

Lesion of the hippocampus selectively enhances LEC’s activity during recognition memory based on familiarity

“…This underlines the robustness of the findings and the fact that this result is independent of experimental conditions. Also, as mentioned previously, even though the role of PER in familiarity has been extensively studied in humans and rodents 7 , 12 – 18 , 39 , evidence for a specific involvement of LEC has been scarce in animals 17 and inexistent in humans. Hence, the extent to which the engagement of LEC and PER during judgments based on familiarity is comparable in healthy subjects or when hippocampal function is compromised was not known.…”

“…mainly based on its strong anatomical ties with PER 7 , 8 while others have attributed this function to HIP in addition to its well-established role in the recollection of episodic events 9 – 11 . Plethora of studies have reported a specific involvement of PER in the familiarity process, especially during spontaneous object recognition memory in rodents and word recognition memory in humans 7 , 8 , 12 – 18 . In contrast, clear empirical evidence for a selective involvement of LEC in familiarity judgements is lacking.…”

Lesion of The Hippocampus Selectively Enhances LEC's Activity During Recognition Memory Based On Familiarity

“…This underlines the robustness of the findings and the fact that this result is independent of experimental conditions. Also, as mentioned previously, even though the role of PER in familiarity has been extensively studied in humans and rodents (Bowles et al, 2007;Bowles et al, 2010;Haskins et al, 2008;Murray, Bussey, & Saksida, 2007;Farovik et al, 2011;Atucha et al, 2017;Köhler and Martin ,2020; see for reviews Brown and Aggleton, 2001;Eichenbaum et al, 2012), evidence for a specific involvement of LEC has been scarce in animals (Atucha et al, 2017) and inexistent in humans. Hence, the extent to which the engagement of LEC and PER during judgments based on familiarity is comparable in healthy subjects or when hippocampal function is compromised was not known.…”

“…single objects, odors etc…) mainly based on its strong anatomical ties with PER (Brown and Aggleton et al, 2001; see Eichenbaum et al, 2007 for a review) while others have attributed this function to HIP in addition to its well-established role in the recollection of episodic events (Squire, 1992;Squire and Zola, 1998;Wixted and Squire, 2011). Plethora of studies have reported a specific involvement of PER in the familiarity process, especially during spontaneous object recognition memory in rodents and word recognition memory in humans (Bowles et al, 2007(Bowles et al, , 2010Farovik et al, 2011;Haskins et al 2008;Murray, Bussey, & Saksida, 2007;Atucha et al, 2017;Köhler and Martin, 2020; see for reviews Brown and Aggleton, 2001;Eichenbaum et al, 2007). In contrast, clear empirical evidence for a selective involvement of LEC in familiarity judgements is lacking.…”

Cognitive Neuroscience Perspectives on Motivation and Learning: Revisiting Self‐Determination Theory

“…As such, it has been postulated to be the nexus of the creation of memories for those individual percepts. This notion is supported by the case of a patient with selective damage to this area, who exhibits specific impairment in feeling familiarity (Köhler & Martin, 2020). In contrast, the hippocampus, a subcortical structure receiving input from the perirhinal cortex, has been identified as a vital locus of memory formation for associations, transitive learning, spatial mapping, and other complex representations (Eichenbaum, 2017).…”