The development of object recognition memory in rhesus macaques with neonatal lesions of the perirhinal cortex

Zeamer, Alyson; Richardson, Ricardo M.; Weiss, Alison R.; Bachevalier, Jocelyne

doi:10.1016/j.dcn.2014.07.002

Cited by 24 publications

(59 citation statements)

References 48 publications

(72 reference statements)

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“…Lesion extents have already been described in detail (see [19]) and are summarized in Table 1. Briefly, the ibotenic acid injections resulted in extensive bilateral damage to the PRh in all cases (average=73.6%, min=67.1%, max=83.3%).…”

Section: Methodsmentioning

confidence: 99%

“…Additionally, there was minor damage to the hippocampus (average=0.8%) in 4 cases, and to the amygdala (average=2.5%) in 3 cases. Figure 1 shows pre-surgical and post-surgical MR images of a representative case (Neo-PRh-2; see also case Neo-PRh-3 illustrated in [19]).…”

Section: Methodsmentioning

confidence: 99%

“…These recognition memory abilities were severely compromised in infant monkeys that had received bilateral neurotoxic damage to the PRh (Neo-PRh) in the first 2 weeks after birth [19]. This memory loss was mild but emerged as early as 1.5 months, became more pronounced in adolescence (18 months), and remained present in adulthood (48 months).…”

Section: Introductionmentioning

confidence: 99%

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Object and spatial memory after neonatal perirhinal lesions in monkeys

Weiss

Bachevalier

2016

Behavioural Brain Research

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The contribution of the perirhinal cortex (PRh) to recognition memory is well characterized in adults, yet the same lesions have limited effect on recognition of spatial locations. Here, we assessed whether the same outcomes will follow when perirhinal lesions are performed in infancy. Monkeys with neonatal perirhinal (Neo-PRh) lesions and control animals were tested in three operant recognition tasks as they reached adulthood: Delayed Nonmatching-to-Sample (DNMS) and Object Memory Span (OMS), measuring object recognition, and Spatial Memory Span (SMS), measuring recognition of spatial locations. Although Neo-PRh lesions did not impact acquisition of the DNMS rule, they did impair performance when the delays were extended from 30s to 600s. In contrast, the same neonatal lesions had no impact on either the object or spatial memory span tasks, suggesting that the lesions impacted the maintenance of information across longer delays and not memory capacity. Finally, the magnitude of recognition memory impairment after the Neo-PRh lesions was similar to that previously observed after adult-onset perirhinal lesions, indicating minimal, or no, functional compensation after the early PRh lesions. Overall, the results indicate that the PRh is a cortical structure that is important for the normal development of mechanisms supporting object recognition memory. Its contribution may be relevant to the memory impairment observed with human cases of temporal lobe epilepsy without hippocampal sclerosis, but not to the memory impairment found in developmental amnesia cases.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Object and spatial memory after neonatal perirhinal lesions in monkeys

Weiss

Bachevalier

2016

Behavioural Brain Research

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“…ERh, entorhinal cortex; AMY, amygdala; HF, hippocampal formation. For complete list, see Zeamer et al (2015). …”

Section: Figurementioning

confidence: 99%

Neonatal perirhinal cortex lesions impair monkeys’ ability to modulate their emotional responses.

Ahlgrim

Raper

Johnson

et al. 2017

Behavioral Neuroscience

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The medial temporal lobe (MTL) is a collection of brain regions best known for their role in perception, memory, and emotional behavior. Within the MTL, the perirhinal cortex (PRh) plays a critical role in perceptual representation and recognition memory, although its contribution to emotional regulation is still debated. Here, rhesus monkeys with neonatal perirhinal lesions (Neo-PRh) and controls (Neo-C) were tested on the Human Intruder (HI) task at 2 months, 4.5 months, and 5 years of age, to assess the role of the PRh in the development of emotional behaviors. The HI task presents a tiered social threat to which typically developing animals modulate their emotional responses according to the level of threat. Unlike animals with neonatal amygdala or hippocampal lesions, Neo-PRh animals were not broadly hyper- or hypo-responsive to the threat presented by the HI task as compared to controls. Instead, Neo-PRh animals displayed an impaired ability to modulate their freezing and anxiety-like behavioral responses according to the varying levels of threat. Impaired transmission of perceptual representation generated by the PRh to the amygdala and hippocampus may explain the animals’ inability to appropriately assess and react to complex social stimuli. Neo-PRh animals also displayed fewer hostile behaviors in infancy and more coo vocalizations in adulthood. Neither stress reactive nor basal cortisol levels were affected by the Neo-PRh lesions. Overall, these results suggest that the PRh is indirectly involved in the expression of emotional behavior, and that effects of Neo-PRh lesions are dissociable from neonatal lesions to other temporal lobe structures.

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“…Neonatal perirhinal lesions in monkeys altered novelty preference across all delays and at all ages tested (i.e. 1.5, 6 and 18 months) and this deficit became more profound as the animals matured (Zeamer & Bachevalier, 2014). Thus, the neurobiological evidence together with the present behavioral findings indicate the emergence of significant changes in functional interactions between the medial temporal cortical areas, such as the perirhinal cortex, and the hippocampus after 6 months of age.…”

Section: Early Developing Recognition Memory Processesmentioning

confidence: 99%

Commentary

Bachevalier

2015

International Journal of Behavioral Development

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Studies investigating the development of memory processes and their neural substrates have flourished over the last two decades. The review by Jabès and Nelson (2015) adds an important piece to our understanding of the maturation of different elements and circuits within the hippocampal system and their association with the progressive development of hippocampal-dependent memory processes in humans. In this accompanying commentary, we explore some additional connections between the nonhuman primate work and the human data, and take the opportunity to highlight some common and additional interpretations of the results. This commentary makes three points: (1) the recognition processes present in the first few days of life may be linked to the early maturation of the medial temporal cortical areas instead of, or in addition to, the early maturation of the subiculum; (2) recent findings on the differential protracted maturation of spatial relational memory processes in monkeys further support the notion proposed by Jabès and Nelson that this protracted development may reflect progressive maturation of the CA1 field of the hippocampus followed by further maturation of CA3/dentate gyrus; (3) finally, further considerations of the differential maturation of the longitudinal hippocampal axis and of the diencephalon are proposed as additional contributors to the refinement of episodic memory functions during development.

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The development of object recognition memory in rhesus macaques with neonatal lesions of the perirhinal cortex

Cited by 24 publications

References 48 publications

Object and spatial memory after neonatal perirhinal lesions in monkeys

Object and spatial memory after neonatal perirhinal lesions in monkeys

Neonatal perirhinal cortex lesions impair monkeys’ ability to modulate their emotional responses.

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