Adaptability to changes in temporal structure is fornix-dependent

Abstract

Recognition memory deficits, even after short delays, are sometimes observed following hippocampal damage. One hypothesis links the hippocampus with processes in updating contextual memory representation. Here, we used fornix transection, which partially disconnects the hippocampal system, and compares the performance of fornix-transected monkeys with normal monkeys on two versions of a delayed-matching-to-position task with short delays. Spatial recognition memory was affected by fornix transection only when the temporal structure of the task changed across trials, while differences in motor control, motivation, perception, or short-term memory were not critical. We attributed the deficit to a compromised ability in tracking changes in task temporal structure.Fornix transection disconnects one of the major input/output pathways of the hippocampus (Saunders and Aggleton 2007). In humans, fornix damage may result in long-term memory loss in recognition (Gaffan and Gaffan 1991;Poreh et al. 2006) and recall (McMackin et al. 1995;Aggleton et al. 2000) whereas short-term/ working memory (STM) is sometimes spared (Scoville and Milner 1957;Cave and Squire 1992;Ryan and Cohen 2004). Similarly, monkeys with lesions of the hippocampal formation performed normally on a delayed nonmatching-to-sample task when the delays were short (≤15 sec) but were impaired at longer delays (.30 sec) (Alvarez et al. 1994), in keeping with the notion that the hippocampal system contributes to the recovery of contextual details in long-term memory (Tsivilis et al. 2008;Vann et al. 2009). However, other evidence has challenged this dissociation (Ranganath and Blumenfeld 2005;Kwok and Macaluso 2015). For example, lesions in the medial temporal lobe (MTL) can impair retention of information across short delays (Jeneson et al. 2012) and the hippocampus exhibits persistent activity during STM maintenance (Chein et al. 2011), indicative of a hippocampal role in STM too. Indeed, some recent neuropsychological studies associate hippocampal disruption with deficits in spatial tasks placing high demands on spatial configural processes even in the absence of any delay (Lee et al. 2005(Lee et al. , 2006, further refuting delaydependent theories.Recent studies have provided one possible account to reconcile these seemingly contradictory results. On the one hand, empirical data from animal studies link temporal order processing to an extended diencephalic-hippocampal system in both rodents and primates (Fortin et al. 2002;Charles et al. 2004), suggesting the hypothesis that hippocampal networks mediate associations between sequential events. On the other hand, human neuroimaging studies have indicated that multivoxel patterns in the hippocampus contain temporal information (Hsieh et al. 2011;Ezzyat and Davachi 2014) and that interevent associative encoding and retrieval is mediated by the hippocampus (DuBrow and Davachi 2014), suggesting that hippocampal processes may play an important role in establishing temporal relationships among events. Pertinently,...

Spatial responses, immediate experience, and memory in the monkey hippocampus

“…By registering each event as it occurs, the hippocampal network continuously tracks the progression of events within an experience. This interpretation of the ongoing neural activity complements research showing that hippocampal lesions impair the ability to monitor recent choices [15,16,50] and to track events across time [11,13,14,20]. …”

“…However, it is critical to note that these studies mark the few examples of hippocampal-dependent spatial cognition. Importantly, processing positional information alone does not seem to rely on the hippocampus [14,18–20] particularly when it can be egocentrically defined from the perspective of the stationary monkey [21]. Instead, the hippocampus seems to be required when spatial relationships between objects in allocentric space must be formed, and when spatially-distinct objects must be linked across time.…”

Dissecting the Fornix in Basic Memory Processes and Neuropsychiatric Disease: A Review

“…Hirsch & Segal, 1972;O'Keefe et al, 1975;Walker & Olton, 1979;Markowska et al, 1989;Murray et al, 1989;Aggleton et al, 1992;Gaffan, 1994;Ennaceur et al, 1996;Ennaceur & Aggleton, 1997;Parker & Gaffan, 1997;Whishaw & Tomie, 1997;Bussey et al, 2000;De Bruin et al, 2001;Easton et al, 2002;Buckley et al, 2004 andKwok, 2006;Kwok & Buckley, 2010;Kwok et al, 2015;Hodgetts et al, 2017Hodgetts et al, , 2018 Traditional Episodic Memory Tasks, e.g. WMS, CVLT, etc.…”

Corticocortical and Thalamocortical Changes in Functional Connectivity and White Matter Structural Integrity after Reward-Guided Learning of Visuospatial Discriminations in Rhesus Monkeys

“…Additionally, the fornix is associated with recollection and recall in MRI studies (Rudebeck et al, 2009;Metzler-Baddeley et al, 2011) and has shown changes in patients with hippocampal lesions (Henson et al, 2016). Interestingly, causal evidence from humans and nonhuman primates further shows that transecting the UF or the fornix impairs cognitive performance in learning and memory tasks (D'Esposito et al, 1995;Aggleton et al, 2000;Gaffan, 2002;Browning and Gaffan, 2008;Tsivilis et al, 2008;Kwok et al, 2015). However, it remains unclear how learning new visuospatial information alters (sub)cortical connectivity, and how, following the loss of subcortical inputs to the cortex, this connectivity is rearranged.…”