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Social context shapes cognitive abilities: associative memories are modulated by fight outcome and social isolation in the crab Neohelice granulata

Authors:
Jimena Santos at University of Buenos Aires
Jimena Santos
Santiago Abel Merlo at University of Buenos Aires
Santiago Abel Merlo
Laura Kaczer at University of Buenos Aires
Laura Kaczer
María Pedreira at University of Buenos Aires
María Pedreira
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Cognitive abilities of an animal can be influenced by distinct social experiences. However, the extent of this modulation has not been addressed in different learning scenarios: are all tasks similarly affected by social experiences? In the present study, we analyzed the effect of social dominance in aversive and appetitive memory processes in the crab Neohelice granulata. In addition, we studied the influence of social isolation on memory ability. Social dominance experiments consisted of an agonistic phase immediately followed by a memory phase. During the agonistic phase, matched pairs of male crabs were staged in 10-min encounters and the dominant or subordinate condition of each member of the dyad was determined. During the memory phase, crabs were trained to acquire aversive or appetitive memory and tested 24 h later. Results showed that the agonistic encounter can modulate long-term memory according to the dominance condition in such a way that memory retention of subordinates results higher than their respective dominant. Remarkably, this result was found for both aversive and appetitive memory tasks. In addition, we found that isolated animals showed no memory retention when compared with animals that remained grouped. Altogether this work emphasizes the importance of social context as a modulator of cognitive abilities.
a Experimental time scale. b Aversive experimental protocol. Training and test: Differences in rectangles colors stand for the light shift between visual danger stimulus (US) trials. c Appetitive experimental protocol. Training and test: the duration of each session and the time of pellet administration in the trained group is specified
a Experimental time scale. b Aversive experimental protocol. Training and test: Differences in rectangles colors stand for the light shift between visual danger stimulus (US) trials. c Appetitive experimental protocol. Training and test: the duration of each session and the time of pellet administration in the trained group is specified
… 
Effect of fight outcome on exploratory activity, reactivity to VDS and aversive memory. a Experimental protocol: Agonistic encounter: A group of animals stablished dominance by confrontations (DOM/SUB) while another group did not fight and remained isolated (CT). The orange bowl-shaped container symbolizes the actometer. Exploratory activity was measured by video tracking. b Exploratory activity: immediately after fight, animals were placed in the actometers and exploratory activity was measured. c Experimental protocol: Agonistic encounter: A group of animals stablished dominance by confrontations (DOM/SUB) while another group did not fight and remained isolated (CT). The orange bowl-shaped container symbolizes the actometer. Black rectangles represent the VDS and stands for aversive memory training and test. d Training session: immediately after fight the trained groups (TR DOM/TR SUB) received a training session of 15 VDS. The control group (CT) received 1 VDS and stayed in the context without stimulation. Training session shows mean animals response level along the 15 VDS trials. Inset: reactivity to the VDS, shows mean animals’ response to the first presentation on the VDS in the training session. e Test session: took place after 24 h, graph shows mean animals response level along the 6 VDS trials in the test session. Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR < CT, memory retention). Group sizes: A, CT: 58, TR-SUB: 58, TR-DOM: 59; B, CT: 32, TR-SUB: 31, TR-DOM: 33
Effect of fight outcome on exploratory activity, reactivity to VDS and aversive memory. a Experimental protocol: Agonistic encounter: A group of animals stablished dominance by confrontations (DOM/SUB) while another group did not fight and remained isolated (CT). The orange bowl-shaped container symbolizes the actometer. Exploratory activity was measured by video tracking. b Exploratory activity: immediately after fight, animals were placed in the actometers and exploratory activity was measured. c Experimental protocol: Agonistic encounter: A group of animals stablished dominance by confrontations (DOM/SUB) while another group did not fight and remained isolated (CT). The orange bowl-shaped container symbolizes the actometer. Black rectangles represent the VDS and stands for aversive memory training and test. d Training session: immediately after fight the trained groups (TR DOM/TR SUB) received a training session of 15 VDS. The control group (CT) received 1 VDS and stayed in the context without stimulation. Training session shows mean animals response level along the 15 VDS trials. Inset: reactivity to the VDS, shows mean animals’ response to the first presentation on the VDS in the training session. e Test session: took place after 24 h, graph shows mean animals response level along the 6 VDS trials in the test session. Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR < CT, memory retention). Group sizes: A, CT: 58, TR-SUB: 58, TR-DOM: 59; B, CT: 32, TR-SUB: 31, TR-DOM: 33
… 
Effect of fight outcome on reactivity to VDS and aversive memory: an analysis of the parametric properties of the stimulus (VDS). a Experimental protocol: Agonistic encounter: animals stablished dominance by confrontations (DOM/SUB). Symbols as Fig. 1a. b–d Training session: immediately after fight the trained groups (TR-DOM/TR-SUB) received a training session of 15 VDS with standard stimulus (b) or strong stimulus (d). The control group (CT-SUB/CT-DOM) received 1 VDS and stayed in the context without stimulation. Training session shows mean response level along the 15 VDS trials. Inset: reactivity to the VDS, shows mean response to the first presentation on the VDS in the training session. c-e Test session: took place after 24 h, graph shows mean response level along the 6 VDS trials in the test session with the standard stimulus (c) or higher stimulus (e). Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR < CT, memory retention). Group sizes: B-C, CT-SUB: 34, TR-SUB: 31, CT-DOM: 40, TR-DOM: 34: D-E, CT-SUB: 22, TR-SUB: 22, CT-DOM: 23, TR-DOM: 22
Effect of fight outcome on reactivity to VDS and aversive memory: an analysis of the parametric properties of the stimulus (VDS). a Experimental protocol: Agonistic encounter: animals stablished dominance by confrontations (DOM/SUB). Symbols as Fig. 1a. b–d Training session: immediately after fight the trained groups (TR-DOM/TR-SUB) received a training session of 15 VDS with standard stimulus (b) or strong stimulus (d). The control group (CT-SUB/CT-DOM) received 1 VDS and stayed in the context without stimulation. Training session shows mean response level along the 15 VDS trials. Inset: reactivity to the VDS, shows mean response to the first presentation on the VDS in the training session. c-e Test session: took place after 24 h, graph shows mean response level along the 6 VDS trials in the test session with the standard stimulus (c) or higher stimulus (e). Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR < CT, memory retention). Group sizes: B-C, CT-SUB: 34, TR-SUB: 31, CT-DOM: 40, TR-DOM: 34: D-E, CT-SUB: 22, TR-SUB: 22, CT-DOM: 23, TR-DOM: 22
… 
Effect of social isolation in the acquisition and retention of an aversive memory. a Experimental protocol: Two pairs of control (CT)—trained (TR) groups: animals that spend a week in isolation in individual containers and animals that remained grouped with 20 crabs per container. Symbols as Fig. 1a. b Training session: after 1 week the trained groups (TR-GROUPED/TR-ISOLATED) received a training session of 15 VDS. Control groups (CT-GROUPED/CT-ISOLATED) received 1 VDS and stayed in the context without stimulation. Training session shows mean response level along the 15 VDS trials. Inset: reactivity to the VDS, shows mean response to the first presentation on the VDS in the training session. c Test session: took place after 24 h, graph shows mean animals response level along the 6 VDS trials in the test session. Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR < CT, memory retention). Group sizes: CT-GROUPED: 31, TR-GROUPED: 32, CT-ISOLATED: 31, TR-ISOLATED: 32
Effect of social isolation in the acquisition and retention of an aversive memory. a Experimental protocol: Two pairs of control (CT)—trained (TR) groups: animals that spend a week in isolation in individual containers and animals that remained grouped with 20 crabs per container. Symbols as Fig. 1a. b Training session: after 1 week the trained groups (TR-GROUPED/TR-ISOLATED) received a training session of 15 VDS. Control groups (CT-GROUPED/CT-ISOLATED) received 1 VDS and stayed in the context without stimulation. Training session shows mean response level along the 15 VDS trials. Inset: reactivity to the VDS, shows mean response to the first presentation on the VDS in the training session. c Test session: took place after 24 h, graph shows mean animals response level along the 6 VDS trials in the test session. Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR < CT, memory retention). Group sizes: CT-GROUPED: 31, TR-GROUPED: 32, CT-ISOLATED: 31, TR-ISOLATED: 32
… 
Fight outcome and modulation of an appetitive memory. a Experimental protocol: Agonistic encounter: animals stablished dominance by confrontations (DOM/SUB). Symbols as Fig. 1a. b Test session: immediately after fight the trained groups (TR-DOM/TR-SUB) received a food pellet. The control group (CT-SUB/ CT-DOM) stayed in the context without stimulation. After 24 h animals were tested measuring exploratory activity by video tracking. Graph shows mean exploratory activity level at test session. Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR > CT, memory retention). Group sizes: CT-SUB: 29, TR-SUB: 32, CT-DOM: 28, TR-DOM: 29
Fight outcome and modulation of an appetitive memory. a Experimental protocol: Agonistic encounter: animals stablished dominance by confrontations (DOM/SUB). Symbols as Fig. 1a. b Test session: immediately after fight the trained groups (TR-DOM/TR-SUB) received a food pellet. The control group (CT-SUB/ CT-DOM) stayed in the context without stimulation. After 24 h animals were tested measuring exploratory activity by video tracking. Graph shows mean exploratory activity level at test session. Data are expressed as mean response level ± S.E. Planned comparisons (LSD): *stands for p < 0.05 (TR > CT, memory retention). Group sizes: CT-SUB: 29, TR-SUB: 32, CT-DOM: 28, TR-DOM: 29
… 
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Animal Cognition (2021) 24:1007–1026
https://doi.org/10.1007/s10071-021-01492-6
ORIGINAL ARTICLE
Social context shapes cognitive abilities: associative memories are
modulated byfight outcome andsocial isolation inthecrab Neohelice
granulata
M.JimenaSantos1,2· SantiagoA.Merlo1,2· LauraKaczer1,2· MariaE.Pedreira1,2
Received: 11 July 2020 / Revised: 9 February 2021 / Accepted: 15 February 2021 / Published online: 31 March 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021
Abstract
Cognitive abilities of an animal can be influenced by distinct social experiences. However, the extent of this modulation
has not been addressed in different learning scenarios: are all tasks similarly affected by social experiences? In the present
study, we analyzed the effect of social dominance in aversive and appetitive memory processes in the crabNeohelice granu-
lata.In addition, we studied the influence of social isolation on memory ability. Social dominance experiments consisted of
an agonistic phase immediately followed by a memory phase. During the agonistic phase, matched pairs of male crabs were
staged in 10-min encounters and the dominant or subordinate condition of each member of the dyad was determined. During
the memory phase, crabs were trained to acquire aversive or appetitive memory and tested 24h later. Results showed that
the agonistic encounter can modulate long-term memory according to the dominance condition in such a way that memory
retention of subordinates results higher than their respective dominant. Remarkably, this result was found for both aversive
and appetitive memory tasks.In addition, we found that isolated animals showed no memory retention when compared
with animals that remained grouped. Altogether this work emphasizes the importance of social context as a modulator of
cognitive abilities.
Keywords Fight outcome· Social isolation· Aversive memory· Appetitive memory· Neohelice granulata· Consolidation·
Exploratory activity
Introduction
Animals live in a complex social environment and the inter-
actions between members of a group mold not only the way
the individuals adapt to limited resources but also their
behavior.
Interaction within members of their species can present
certain advantages and disadvantages. On the one hand, they
can detect/repel predators more easily, defend better, locate
food and resources (Nelson 2005). On the other hand, as
resources are generally limited, this could lead to compe-
tition between members of a group (Huntingforda 2013).
Thus, agonistic interactions appear as a consequence of a
conflict arising in terms of resource acquisition (food, terri-
tory, access to couple) which is ultimately associated with
individual fitness (Arnott and Elwood 2009; Eggert etal.
2008).
In the last years, interest in studying how social context
can shape behavior has increased. Several reports revealed
that individual dominance status can influence other non-
social behaviors (Hofmann etal. 1999; Keeney and Hogg
1999; Maruska and Fernald 2012; May and Mercier 2007;
Robson and Miles 2000; Yeh etal. 1996, 1997). For instance,
in sea lobsters, an animal´s response to a tactile stimulus
differed according to its status: dominants presented an ori-
entation response towards it, while subordinates elicited an
escape response (Song etal. 2006). Further, in an African
cichlid fish, sensorimotor gating of startle behavior, a phe-
nomenon associated with information processing, showed
Laura Kaczer and Maria E. Pedreira have contributed equally to
this work.
* Maria E. Pedreira
mpedreira@fbmc.fcen.uba.ar
1 Instituto de Fisiología, Biología Molecular y Neurociencias
(IFIBYNE)-CONICET, CONICET, 1428BuenosAires,
Argentina
2 Facultad de Ciencias Exactas y Naturales, Universidad de
Buenos Aires, BuenosAires, Argentina
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Recently a link has been reported between spatial memory retention, a critical element for mating success, and the ability to acquire and defend a territory, indicating a key role for cognition in mating. 15 Using Neohelice granulata, Santos et al., 2021, 16 highlight the social context as a modulator of cognitive abilities; the fight outcome between two male crabs modulates associative memories, and long-term memory retention of subordinates is higher than that of their respective dominant. This suggests a possible link between long-term memory retention level and the capacity to tackle agonistic encounters between Neohelice granulata males, which is one of the strategies that affect mating success during the reproductive season. ...
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... Lack of social stimuli can have detrimental effects in species with high affectionate requirements (Harlow et al., 1965;Grippo et al., 2007;Christiansen et al., 2021), while it may have less effects in solitary or facultatively social species (Stowe et al., 2005;Riley et al., 2017). Belonging to a social group may also have beneficial effects on cognitive performance, as shown in wild as well as captive-reared birds (Ashton et al., 2018;Langley et al., 2018), crabs (Santos et al. 2021), and fish (Brandão et al., 2015;Ausas et al. 2019), but effects are not ubiquitous in the animal kingdom (e.g. Riley et al. 2018). ...
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