Research Article: Multisensory guided associative learning in healthy humans

Date Published: March 12, 2019

Publisher: Public Library of Science

Author(s): Gabriella Eördegh, Attila Őze, Balázs Bodosi, András Puszta, Ákos Pertich, Anett Rosu, György Godó, Attila Nagy, Bernadette Ann Murphy.


Associative learning is a basic cognitive function by which discrete and often different percepts are linked together. The Rutgers Acquired Equivalence Test investigates a specific kind of associative learning, visually guided equivalence learning. The test consists of an acquisition (pair learning) and a test (rule transfer) phase, which are associated primarily with the function of the basal ganglia and the hippocampi, respectively. Earlier studies described that both fundamentally-involved brain structures in the visual associative learning, the basal ganglia and the hippocampi, receive not only visual but also multisensory information. However, no study has investigated whether there is a priority for multisensory guided equivalence learning compared to unimodal ones. Thus we had no data about the modality-dependence or independence of the equivalence learning. In the present study, we have therefore introduced the auditory- and multisensory (audiovisual)-guided equivalence learning paradigms and investigated the performance of 151 healthy volunteers in the visual as well as in the auditory and multisensory paradigms. Our results indicated that visual, auditory and multisensory guided associative learning is similarly effective in healthy humans, which suggest that the acquisition phase is fairly independent from the modality of the stimuli. On the other hand, in the test phase, where participants were presented with acquisitions that were learned earlier and associations that were until then not seen or heard but predictable, the multisensory stimuli elicited the best performance. The test phase, especially its generalization part, seems to be a harder cognitive task, where the multisensory information processing could improve the performance of the participants.

Partial Text

Associative learning is a basic cognitive function by which discrete and often different percepts will be linked together. It contributes to several cognitive tasks, i.e. classical conditioning [1], latent inhibition [2] and sensory preconditioning [3]. Catherine E. Myers and co-workers developed a learning paradigm (Rutgers Acquired Equivalence Test, also known as the fish-face paradigm) that can be applied to investigate a specific kind of associative learning, which is visually guided equivalence learning [4]. This test can be divided into two main phases. In the acquisition phase, the subjects are asked to associate two different visual stimuli as the computer provides information about the correctness of the responses. After that in the test phase the subjects receive no feedback about the correctness of their choices. In the test phase, beside the stimulus pairs learned earlier (retrieval part), hitherto not encountered but predictable associations (generalization part) are also presented. A substantial advantage of this test is that well-circumscribed brain structures play the main role in different phases of the test. Optimal performance in the acquisition phase appears to depend mainly on the integrity of the basal ganglia, whereas performance in the test phase (both retrieval and generalization) has been linked to the integrity of the hippocampal region [4, 5]. Our research group has a particular interest in the sensorimotor and cognitive functions of the basal ganglia and has studied with this paradigm since 2006, mostly to assess the development of visually guided associative learning [6] and to examine the progress in various conditions, from Alzheimer’s disease to migraines [7–9]. It is well known from earlier studies that both brain structures fundamentally involved in visual associative learning, the basal ganglia and the hippocampi, receive not only visual but also multisensory information [10–13]. Multimodal information could be more informative than a unimodal stimulus from the environment [14, 15]. Probably because of the merging of senses, multisensority has a priority in spatial orientation and in recognizing objects and events from the multisensory environment [14–16]. Multisensory integration occurs at different levels of brain functions. It can be observed at the cellular level [17–20] in several brain regions such as the superior colliculus [21], basal ganglia [11, 22] the cortex [23], and the hippocampus [24] or on the behavioral level [25, 26]. It can occur between two or three different modalities, for example auditory and visual [27, 28], visual and vestibular [29], auditory and tactile [30], or auditory, visual and somatosensory [11, 31, 32].

Altogether 151 healthy volunteers participated in the study. Only a small minority of the participants (7/151) did not complete all three (visual, auditory, multisensory) paradigms. All of the participants could complete the visual paradigm, one of them could not learn the auditory, and six of them could not learn the multisensory associations. Only the performance and RT of those participants who completed all the three paradigms were further analyzed. After the further exclusion of the extreme outliers, 141 volunteers will be analyzed in detail (nmale = 41, age: 31.21±11.51 years, range: 18–72 years). The outliers were determined as a value above the mean +3SD (by the trial number in one of the paradigms).

The Rutgers Acquired Equivalence Test [4] was originally developed in order to learn about the visually guided associative learning of neurological patients with basal ganglia and hippocampus dysfunction. The test was applied later in cases of psychiatric disorders [41] and also to healthy subjects [6, 42]. Although both the basal ganglia and the hippocampi process not only visual but also multisensory information [10–13] the multisensory guided acquired equivalence learning had not been investigated before. As we recognized this absence we developed a multisensory (audiovisual) version of the associative learning test and were the first to investigate the basal ganglia and hippocampus mediated multisensory guided associative learning in healthy humans. We have to mention here that the aim of the study was not to measure directly the contribution of the involved structures to the paradigms. Thus, we could draw only indirect conclusions about the contribution of the basal ganglia and the hippocampi to the learning paradigms based on our psychophysical results and the results of previous publications in this field [4, 5, 7, 8]. This is a clear psychophysical study, which investigates the performance and the RT of healthy volunteers in different sensory guided associative learning paradigms.




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