Adult neurogenesis promotes efficient, nonspecific search strategies in a spatial alternation water maze task

Abstract

Goal-directed navigation requires learning strategies that are efficient and minimize costs. In some cases it may be desirable to flexibly adjust behavioral responses depending on the cues that vary from one episode to the next. In others, successful navigation might be achieved with inflexible, habit-like responses that reduce cognitive load. Adult neurogenesis is believed to contribute to the spatial processing functions of the hippocampus, particularly when behavioral flexibility is required. However, little is known about the role of neurogenesis in spatial navigation when goals are unpredictable or change according to certain rules. We hypothesized that neurogenesis is necessary in a spatial navigation task that involves different patterns of reinforcement. Intact and neurogenesis-deficient rats were trained to escape to one of two possible platform locations in a spatial water maze. The platform either repeated in the same location for all trials in a day, alternated between two locations across trials, or randomly moved between the two locations. Neurogenesis selectively enhanced escape performance in the alternating condition, but not by improving platform choice accuracy. Instead, neurogenesis-intact rats made fewer search errors and developed an efficient habit-like strategy where they consistently swam to a preferred location. If the platform was not present, they proceeded to the other possible location. In contrast, neurogenesis-deficient rats were indecisive and navigationally less-efficient. Thus, in conditions where goals follow a predictable spatiotemporal pattern, adult neurogenesis promotes the adoption of navigation strategies that are spatially nonspecific but, nonetheless, accurate and efficient.

Inhibiting adult neurogenesis differentially affects spatial learning in females and males

“…Temperature-dependent spatial functions of newborn neurons. While some have reported acquisition and short term reference memory deficits in the spatial water maze in neurogenesis-deficient animals (14,69,72), a majority of studies have found intact spatial learning (2,6,7,15,(17)(18)(19)(20)(21)(22), raising questions about the necessity of adult neurogenesis for spatial learning. Our findings indicate that the degree of stress and/or aversiveness present at the time of learning is critical (as suggested by ( 73)).…”

“…Adult hippocampal neurogenesis has been implicated in many of the mnemonic functions of the hippocampus, including memory for temporal events (1-3), locations (4), contexts (5,6), objects (7,8) and conspecifics (9), as well as the consolidation (10,11) and forgetting (12) of memory. While spatial memory functions may be particularly apparent in conditions that maximize conflict or interference, such as when a goal changes location (13)(14)(15)(16), it is notable that many of studies have failed to find a role for new neurons in learning and short-term reference memory in the spatial water maze, a task that is highly sensitive to hippocampal disruption (2,6,7,(17)(18)(19)(20)(21)(22).…”

Disruption of NREM sleep and sleep-related spatial memory consolidation in mice lacking adult hippocampal neurogenesis

“…Consistent with former studies, we found that Cyclin D2 −/− mice were not generally impaired in learning the spatial memory task, but rarely used the most efficient hippocampus-dependent search strategies and showed a lower route efficiency on day 2 and 3-after the first post-learning sleep. Route efficiency and search strategy depend on the use of a cognitive map encoded in the hippocampal formation 46,47 . The use of the most sophisticated search strategies has been shown to be a reliable qualitative parameter for hippocampus-dependent learning 39,47 .…”

“…Route efficiency and search strategy depend on the use of a cognitive map encoded in the hippocampal formation 46,47 . The use of the most sophisticated search strategies has been shown to be a reliable qualitative parameter for hippocampus-dependent learning 39,47 . Accordingly, age-dependent decline of adult neurogenesis is associated with less frequent use of hippocampal search strategies 48 .…”

Loss of α7 nicotinic acetylcholine receptors in GABAergic interneurons causes sex-dependent impairments in postnatal neurogenesis and cognitive and social behavior

“…Together these findings suggest a possible relationship between the level of postnatal neurogenesis and overall spatial performance. Postnatal hippocampal neurogenesis has been shown to have little role in short term spatial memory in the water maze (Snyder et al 2005), however it does impact spatial search strategies (Yu et al 2019). The spatial impairment in the cKO mice could also be due to more direct effects of aberrant cholinergic signaling on encoding, retrieval and task performance.…”