Abstract:HighlightsResults of object-in-context experiments can be influenced by relative recency.Data from two experiments presented supporting this suggestion.This may complicate interpretation of results of object-in-context experiments.Recommendations are made on how to address this.Results consistent with an associative account of recognition memory.
“…Automated tracking of exploratory activity was conducted with ANY-maze software (version 4.5; Stoelting; RRID:SCR_014289). The tracking protocol used was similar to that in previous studies (Tam et al, 2014, 2015, 2016). For each video file, the 20 cm × 20 cm floor of the arena was outlined in ANY-maze, and 2 7 cm × 7 cm notional zones were placed at the corners of the arena where the objects were located.…”
Circadian rhythms optimize physiology and behavior to the varying demands of the 24 h day. The master circadian clock is located in the suprachiasmatic nuclei (SCN) of the hypothalamus and it regulates circadian oscillators in tissues throughout the body to prevent internal desynchrony. Here, we demonstrate for the first time that, under standard 12 h:12 h light/dark (LD) cycles, object, visuospatial, and olfactory recognition performance in C57BL/6J mice is consistently better at midday relative to midnight. However, under repeated exposure to constant light (rLL), recognition performance becomes desynchronized, with object and visuospatial performance better at subjective midday and olfactory performance better at subjective midnight. This desynchrony in behavioral performance is mirrored by changes in expression of the canonical clock genes Period1 and Period2 (Per1 and Per2), as well as the immediate-early gene Fos in the SCN, dorsal hippocampus, and olfactory bulb. Under rLL, rhythmic Per1 and Fos expression is attenuated in the SCN. In contrast, hippocampal gene expression remains rhythmic, mirroring object and visuospatial performance. Strikingly, Per1 and Fos expression in the olfactory bulb is reversed, mirroring the inverted olfactory performance. Temporal desynchrony among these regions does not result in arrhythmicity because core body temperature and exploratory activity rhythms persist under rLL. Our data provide the first demonstration that abnormal lighting conditions can give rise to temporal desynchrony between autonomous circadian oscillators in different regions, with different consequences for performance across different sensory domains. Such a dispersed network of dissociable circadian oscillators may provide greater flexibility when faced with conflicting environmental signals.SIGNIFICANCE STATEMENT A master circadian clock in the suprachiasmatic nuclei (SCN) of the hypothalamus regulates physiology and behavior across the 24 h day by synchronizing peripheral clocks throughout the brain and body. Without the SCN, these peripheral clocks rapidly become desynchronized. Here, we provide a unique demonstration that, under lighting conditions in which the central clock in the SCN is dampened, peripheral oscillators in the hippocampus and olfactory bulb become desynchronized, along with the behavioral processes mediated by these clocks. Multiple clocks that adopt different phase relationships may enable processes occurring in different brain regions to be optimized to specific phases of the 24 h day. Moreover, such a dispersed network of dissociable circadian clocks may provide greater flexibility when faced with conflicting environmental signals (e.g., seasonal changes in photoperiod).
“…Automated tracking of exploratory activity was conducted with ANY-maze software (version 4.5; Stoelting; RRID:SCR_014289). The tracking protocol used was similar to that in previous studies (Tam et al, 2014, 2015, 2016). For each video file, the 20 cm × 20 cm floor of the arena was outlined in ANY-maze, and 2 7 cm × 7 cm notional zones were placed at the corners of the arena where the objects were located.…”
Circadian rhythms optimize physiology and behavior to the varying demands of the 24 h day. The master circadian clock is located in the suprachiasmatic nuclei (SCN) of the hypothalamus and it regulates circadian oscillators in tissues throughout the body to prevent internal desynchrony. Here, we demonstrate for the first time that, under standard 12 h:12 h light/dark (LD) cycles, object, visuospatial, and olfactory recognition performance in C57BL/6J mice is consistently better at midday relative to midnight. However, under repeated exposure to constant light (rLL), recognition performance becomes desynchronized, with object and visuospatial performance better at subjective midday and olfactory performance better at subjective midnight. This desynchrony in behavioral performance is mirrored by changes in expression of the canonical clock genes Period1 and Period2 (Per1 and Per2), as well as the immediate-early gene Fos in the SCN, dorsal hippocampus, and olfactory bulb. Under rLL, rhythmic Per1 and Fos expression is attenuated in the SCN. In contrast, hippocampal gene expression remains rhythmic, mirroring object and visuospatial performance. Strikingly, Per1 and Fos expression in the olfactory bulb is reversed, mirroring the inverted olfactory performance. Temporal desynchrony among these regions does not result in arrhythmicity because core body temperature and exploratory activity rhythms persist under rLL. Our data provide the first demonstration that abnormal lighting conditions can give rise to temporal desynchrony between autonomous circadian oscillators in different regions, with different consequences for performance across different sensory domains. Such a dispersed network of dissociable circadian oscillators may provide greater flexibility when faced with conflicting environmental signals.SIGNIFICANCE STATEMENT A master circadian clock in the suprachiasmatic nuclei (SCN) of the hypothalamus regulates physiology and behavior across the 24 h day by synchronizing peripheral clocks throughout the brain and body. Without the SCN, these peripheral clocks rapidly become desynchronized. Here, we provide a unique demonstration that, under lighting conditions in which the central clock in the SCN is dampened, peripheral oscillators in the hippocampus and olfactory bulb become desynchronized, along with the behavioral processes mediated by these clocks. Multiple clocks that adopt different phase relationships may enable processes occurring in different brain regions to be optimized to specific phases of the 24 h day. Moreover, such a dispersed network of dissociable circadian clocks may provide greater flexibility when faced with conflicting environmental signals (e.g., seasonal changes in photoperiod).
“…On each recognition trial, videos were recorded during the sample and test phases. Automated tracking was subsequently conducted with the ANY- maze software (version 4.5; Stoelting, Wood Dale, IL) as in previous studies [35–37]. Figure 1.The effect of visual context change on object recognition performance depends on rods/cones but not melanopsin.…”
Acute light exposure exerts various effects on physiology and behaviour. Although the effects of light on brain network activity in humans are well demonstrated, the effects of light on cognitive performance are inconclusive, with the size, as well as direction, of the effect depending on the nature of the task. Similarly, in nocturnal rodents, bright light can either facilitate or disrupt performance depending on the type of task employed. Crucially, it is unclear whether the effects of light on behavioural performance are mediated via the classical image-forming rods and cones or the melanopsin-expressing photosensitive retinal ganglion cells. Here, we investigate the modulatory effects of light on memory performance in mice using the spontaneous object recognition task. Importantly, we examine which photoreceptors are required to mediate the effects of light on memory performance. By using a cross-over design, we show that object recognition memory is disrupted when the test phase is conducted under a bright light (350 lux), regardless of the light level in the sample phase (10 or 350 lux), demonstrating that exposure to a bright light at the time of test, rather than at the time of encoding, impairs performance. Strikingly, the modulatory effect of light on memory performance is completely abolished in both melanopsin-deficient and rodless–coneless mice. Our findings provide direct evidence that melanopsin-driven and rod/cone-driven photoresponses are integrated in order to mediate the effect of light on memory performance.
“…A parallel effect was found: switching A and B would create a mismatch and increase viewing of this first-presented image pair, thus enhancing the recency effect, while switching C and D would do the opposite. In fact a complementary effect has been reported in rodents by Tam et al (2015) , while investigating the influence of recency on performance on a commonly used variant of the object-in-place task in which animals are first exposed to object A in context x , and then object B in context y , before being tested with A and B in either x or y . Animals typically explore B more in x , and A more in y , demonstrating memory for where these objects were presented in preexposure, and this is usually taken as evidence of an object-in-place effect.…”
Section: Discussionmentioning
confidence: 74%
“…Specifically, during sample presentations the various target images may also become associated with the surrounding context, which acquires the ability to prime those images’ elements directly into the A2 state, and this effect is superimposed on the relative recency effect (cf. Tam et al, 2015 ). We manipulated this process, by accompanying each A and B image with its own context stimulus, x or y (a trial-unique image of a colorful maritime flag).…”
Section: Methodsmentioning
confidence: 99%
“…However, we are unaware of any demonstrations of relative recency using eye-tracking, and so to provide such a demonstration was the first aim of the present experiments. The second was to evaluate our SOP interpretation of these phenomena, which has been the subject of object recognition experiments with rodents (e.g., Tam, Bonardi, & Robinson, 2015 ; Tam, Robinson, Jennings, & Bonardi, 2014 ; Whitt, Haselgrove, & Robinson, 2012 ; Whitt & Robinson, 2013 ).…”
We report 2 eye-tracking experiments with human variants of 2 rodent recognition memory tasks,
relative recency
and
object-in-place
. In Experiment 1 participants were sequentially exposed to 2 images,
A
then
B
, presented on a computer display. When subsequently tested with both images, participants biased looking toward the first-presented image
A
: the relative recency effect. When contextual stimuli
x
and
y
, respectively, accompanied
A
and
B
in the exposure phase (
xA
,
yB
), the recency effect was greater when
y
was present at test, than when
x
was present. In Experiment 2 participants viewed 2 identical presentations of a 4-image array,
ABCD
, followed by a test with the same array, but in which one of the pairs of stimuli exchanged position (
BA
CD or
AB
DC
). Participants looked preferentially at the displaced stimulus pair: the object-in-place effect. Three further conditions replicated Experiment 1’s findings: 2 pairs of images were presented one after the other (
AB
followed by
CD
); on a test with
AB
and
CD
, relative recency was again evident as preferential looking at
AB
. Moreover, this effect was greater when the positions of the first-presented
A
and
B
were exchanged between exposure and test (
BA
CD), compared with when the positions of second-presented
C
and
D
were exchanged (
AB
DC
). The results were interpreted within the theoretical framework of the Sometime Opponent Process model of associative learning (
Wagner, 1981
).
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