Elsevier

Neuroscience Research

Volume 93, April 2015, Pages 136-143
Neuroscience Research

Individual variability in visual discrimination and reversal learning performance in common marmosets

https://doi.org/10.1016/j.neures.2014.10.001Get rights and content

Highlights

  • We trained 42 marmosets in visual discrimination and reversal learning.

  • In 87% of measurements, they showed high performance with 95% correct responses.

  • We quantified their learning processes with two statistical measures.

  • With these measures, some features of learning set formation could be elucidated.

  • Sex and age had no effect on learning as far as adolescents and young adults were used.

Abstract

Detailed information about the characteristics of learning behavior in marmosets is useful for future marmoset research. We trained 42 marmosets in visual discrimination and reversal learning. All marmosets could learn visual discrimination, and all but one could complete reversal learning, though some marmosets failed to touch the visual stimuli and were screened out. In 87% of measurements, the final percentage of correct responses was over 95%. We quantified performance with two measures: onset trial and dynamic interval. Onset trial represents the number of trials that elapsed before the marmoset started to learn. Dynamic interval represents the number of trials from the start before reaching the final percentage of correct responses. Both measures decreased drastically as a result of the formation of discrimination learning sets. In reversal learning, both measures worsened, but the effect on onset trial was far greater. The effects of age and sex were not significant as far as we used adolescent or young adult marmosets. Unexpectedly, experimental circumstance (in the colony or isolator) had only a subtle effect on performance. However, we found that marmosets from different families exhibited different learning process characteristics, suggesting some family effect on learning.

Introduction

Common marmosets (Callithrix jacchus) have recently been used as nonhuman primate models for various human diseases in neuroscience research (Mansfield, 2003, ‘t Hart et al., 2012, Kishi et al., 2014). Efficient and stable methods to assess cognitive functions are essential in such models. Visual discrimination and reversal learning have often been used in marmoset research (Cotterman et al., 1956, Ridley et al., 1981, Ridley et al., 1986, Ridley et al., 1993, Roberts et al., 1988, Roberts et al., 1992, Dias et al., 1996, Fine et al., 1997, Harder et al., 1998, Smith et al., 1999, Clarke et al., 2004, Clarke et al., 2005, Clarke et al., 2007, Clarke et al., 2008, Clarke et al., 2011, Pryce et al., 2004, Man et al., 2009, Rygula et al., 2010), and they are applicable to a wide range of investigations of different processes in reinforcement learning, such as attention, value estimation, and memory formation (Izquierdo and Jentsch, 2012, Gilmour et al., 2013, Klanker et al., 2013). In rodent studies, visual discrimination and reversal learning have been widely used, and the established protocols enable new researchers to easily initiate their experiments (e.g., Horner et al., 2013). In marmoset studies, the use of visual discrimination and reversal learning has been limited to a small number of laboratories, likely because detailed information about experimental procedures and characteristics of learning behavior in marmosets have not been reported. To our knowledge, no previous studies have systematically examined individual variability in the learning performance of marmosets.

In our laboratory, over 40 marmosets have thus far been trained in visual discrimination and reversal learning. We attempted to quantify their performance. To this end, appropriate measures for the animals’ performance are necessary. The most commonly used measure is the total number of trials or errors until the animal achieves a certain criterion. However, we did not adopt this measure in the present study, as a criterion has typically been determined arbitrarily and such a measure has therefore differed across studies. Instead, we adopted more objective and informative measures based on a learning curve, which represents the probability of a correct response as a function of trial number.

Currently, there are two popular methods to assess performance from the learning curve for each subject (Gallistel et al., 2004, Smith et al., 2004), both of which have advantages over conventional methods (e.g., the moving average method). One is a model-based method proposed by Smith et al. (2004) in which a state-space smoothing algorithm is used and the estimated learning curve is gradual. The other is a purely descriptive method proposed by Gallistel et al. (2004) in which change points are determined on a cumulative response curve by a recursive algorithm and the estimated learning curve is given as a staircase function. As the latter method is sensitive to an early onset and abrupt changes in learning curves, the authors found that different onsets and abrupt rises can be detected in individual learning curves, even in the gradual group-average learning curve. In the present study, we adopted the method of Gallistel et al. (2004) and used two representative values—onset trial and dynamic interval—as measures of individual learning performance.

To determine factors that affect performance, we examined the effects of age, sex, and experimental circumstance (in a colony or an isolator rack) on performance. These factors would be considered during experiment planning and subject selection. In addition, we compared the performance of subjects from different families to examine whether a family factor might affect learning behavior.

Section snippets

Subjects

Forty-two naïve adolescent and young adult common marmosets (C. jacchus; 24 males and 18 females, aged 1 year, 7 months to 4 years, 3 months) were used in this study (Table 1). Subjects were born and reared at the Primate Research Institute, Kyoto University. Behavioral experiments were conducted in an individual cage placed in a colony or an isolator rack system (Natsume Seisakusho Co. Ltd., Japan) between 13:00 and 16:00 on weekdays. Subjects were fed 30 g of New World monkey pellets once

The ratio of successfully learned marmosets

Of 42 marmosets, 37 (88%) learned to touch a visual stimulus on the screen in the pre-training (Table 1). Two of the five dropouts (nos. 38 and 39) would not touch the stimulus at the initial stage of the pre-training for more than 10 days. The remaining three dropouts (nos. 40–42) actually touched the stimulus but could not improve their touching methods in the 2-week pre-training. Thus, we trained 37 marmosets in visual discrimination learning, in which all marmosets succeeded. We then

Discussion

In this study, we quantified the performance of more than 40 adolescent and young adult marmosets in visual discrimination and reversal learning. We successfully elucidated some characteristics of marmoset learning ability.

As visual discrimination and reversal learning are often used to assess prefrontal functions, including perseveration and impulsive behavior, the learning statistics presented here are useful for many researchers. Based on these data, all marmosets that learned to touch the

Conclusions

Almost all marmosets could complete visual discrimination and reversal learning. Only one marmoset failed to complete reversal learning. They showed very high performance, with over 95% correct responses in 87% of measurements, and over 90% in 98% of measurements. Such high performance can make the experimental system for marmosets sensitive to the effects of experimental manipulations. With two measures independent of arbitrary criteria, we successfully quantified their learning processes. As

Acknowledgements

This work was partially carried out under the SRPBS from MEXT to KN. This work was partially supported by Cooperative Research Projects for marmoset research to KN.

References (36)

  • A.G. Smith et al.

    The dopamine D3/D2 receptor agonist 7-OH-DPAT induces cognitive impairment in the marmoset

    Pharmacol. Biochem. Behav.

    (1999)
  • A. Takemoto et al.

    Development of a compact and general-purpose experimental apparatus with a touch-sensitive screen for use in evaluating cognitive functions in common marmosets

    J. Neurosci. Methods

    (2011)
  • B.A. ‘t Hart et al.

    The marmoset monkey: a multi-purpose preclinical and translational model of human biology and disease

    Drug Discov. Today

    (2012)
  • C. Yokoyama et al.

    Increase in reaction time for solving problems during learning-set formation

    Behav. Brain Res.

    (2004)
  • H.F. Clarke et al.

    Cognitive inflexibility after prefrontal serotonin depletion

    Science

    (2004)
  • H.F. Clarke et al.

    Dopamine, but not serotonin, regulates reversal learning in the marmoset caudate nucleus

    J. Neurosci.

    (2011)
  • H.F. Clarke et al.

    Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex

    J. Neurosci.

    (2008)
  • H.F. Clarke et al.

    Prefrontal serotonin depletion affects reversal learning but not attentional set shifting

    J. Neurosci.

    (2005)
  • Cited by (21)

    • The marmoset as a model for investigating the neural basis of social cognition in health and disease

      2022, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      A possible contributory factor to females’ preference to engage in habitual behaviour could be differences in the OFC/striatal dopaminergic system, which is an area that can be influenced by circulating oestrogen levels (Lacreuse et al., 2014; LaClair and Lacreuse, 2016; Shams et al., 2016; Brzezinski-Sinai and Brzezinski, 2020; Veselic et al., 2020). Interestingly, both Takemoto et al. (2015) and Ash et al. (2020) reported that there were no sex differences in reversal learning in adolescent marmosets. The discrepancy between the previous studies and the Takemoto and Ash studies can be attributed to the latter studies using younger marmosets.

    • Sex differences in cognitive aging: a 4-year longitudinal study in marmosets

      2022, Neurobiology of Aging
      Citation Excerpt :

      Reversal learning is a test of executive function that assesses cognitive flexibility, or the ability to adapt to changing reward-stimulus contingencies. Reversal learning has been well studied in NHPs including marmosets (Kangas et al., 2016; LaClair and Lacreuse, 2016; Lacreuse et al., 2014a; Munger et al., 2017; Pryce et al., 2004; Ridley et al., 1981; Sadoun et al., 2019; Strasser and Burkart, 2012; Takemoto et al., 2015) and involves a network of brain regions including the orbitofrontal cortex, caudate and striatum (Clarke et al., 2005; Clarke et al., 2011; Collins et al., 2000; Jackson et al., 2018; Roberts et al., 1990). In year 1, a subset of monkeys were also tested on intradimensional/extradimensional set shifting (n = 17) (Laclair et al., 2019), and progressive ratio (n = 16) (Carlotto, unpublished results) but these tests were not administered in subsequent years and are not reported here.

    • Key periods of cognitive decline in a nonhuman primate model of cognitive aging, the common marmoset (Callithrix jacchus)

      2019, Neurobiology of Aging
      Citation Excerpt :

      OT is thus a learning parameter that reflects the number of trials needed to exceed the chance level. The AT was the trial from which an asymptotic level of performance was reached (Takemoto et al., 2015). The dynamic interval (DI) was considered as the number of trials between OT and AT, corresponding to a measure of a transition from a chance level with unconditioned state to a conditioned learning.

    • Development of stereotaxic recording system for awake marmosets (Callithrix jacchus)

      2018, Neuroscience Research
      Citation Excerpt :

      The present stereotaxic recording system is suitable for neuronal recording during task performance of limb and oculomotor movements, since marmosets can move their hands freely and their fixed-heads allow us to easily track their eye movements. Marmosets can learn not only simple motor tasks (Tia et al., 2017) but also various types of tasks to assess cognitive functions, such as visual discrimination (Maclean et al., 2001; Takemoto et al., 2015), reversal learning (Clarke et al., 2005; Rygula et al., 2010; Takemoto et al., 2015) and decision-making (Tokuno and Tanaka, 2011). Thus, neural mechanisms underlying motor control and cognitive functions can be investigated in marmosets by using the present stereotaxic recording system.

    View all citing articles on Scopus
    1

    These authors contributed equally to this work.

    View full text