Is there “neural efficiency” during the processing of visuo-spatial information in male humans? An EEG study

Abstract

More intelligent persons (high IQ) typically present a higher cortical activity during tasks requiring the encoding of visuo-spatial information, namely higher alpha (about 10 Hz) event-related desynchronization (ERD; Doppelmayr et al., 2005 [23]). The opposite is true (“neural efficiency”) during the retrieval of the encoded information, as revealed by both lower alpha ERD and/or lower theta (about 5 Hz) event-related synchronization (ERS; Grabner et al., 2004 [19]). To reconcile these contrasting results, here we evaluated the working hypothesis that more intelligent male subjects are characterized by a high cortical activity during the encoding phase. This deep encoding would explain the relatively low cortical activity for the retrieval of the encoded information. To test this hypothesis, electroencephalographic (EEG) data were recorded in 22 healthy young male volunteers during visuo-spatial information processing (encoding) and short-term retrieval of the encoded information. Cortical activity was indexed by theta ERS and alpha ERD. It was found that the higher the subjects’ total IQ, the stronger the frontal theta ERS during the encoding task. Furthermore, the higher the subjects’ total IQ, the lower the frontal high-frequency alpha ERD (about 10–12 Hz) during the retrieval task. This was not true for parietal counterpart of these EEG rhythms. These results reconcile previous contrasting evidence confirming that more intelligent persons do not ever show event-related cortical responses compatible with “neural efficiency” hypothesis. Rather, their cortical activity would depend on flexible and task-adapting features of frontal activation.

Introduction

Previous neuroimaging studies using positron emission tomography (PET), single photon emission computed tomography (SPECT), and functional magnetic resonance imaging (fMRI) have shown that more intelligent subjects present a weaker fronto-parietal activation during cognitive tasks [1], [2], [3], [4], [5], [6], [7], [8], [9]. To explain these data, it has been proposed the so-called “neural efficiency” hypothesis, which postulates a more efficient brain function in brighter as compared to less intelligent individuals [1], [10]. Other neuroimaging evidence challenged this hypothesis, showing that fronto-parietal cortical activation during cognitive tasks was stronger in more intelligent subjects [11], [12].

To shed light on the physiological mechanism at the basis of the “neural efficiency” hypothesis, event-related changes in power of electroencephalographic (EEG) rhythms at about 4–7 Hz (theta) and 8–12 Hz (alpha) were used. Cortical activity accompanying cognitive and motor tasks is typically associated with a percentage increase of power of theta rhythms (theta event-related synchronization, ERS) and with a percentage decrease of power of resting alpha rhythms (alpha event-related desynchronization, ERD: [13]). In line with the “neural efficiency” hypothesis, it has been shown that more intelligent persons (high IQ) present a lower alpha ERD and/or a lower theta ERS during different types of cognitive tasks [14], [15], [16], [17], [18], [19], [20], [21]. A negative relationship between the alpha ERD and intelligence has been also observed in individuals with high domain-specific skills such as chess players, etc. [22].

Several EEG studies have challenged the “neural efficiency” hypothesis. During a difficult verbal-semantic task (no short-term memory demands), an increase of the theta ERS has been shown in intelligent persons engaged in encoding tasks [23], [24].

The contrasting results regarding the “neural efficiency” hypothesis could be due to different reasons. The mentioned studies employed tasks with marked differences in the stimulus features, task structure, and cognitive processes (i.e. encoding, imagery, and retrieval). Furthermore, more intelligent persons are characterized by high cortical activity when they perceive and work on the external stimuli to be memorized (encoding) as revealed by theta ERS (at odds with “neural efficiency” hypothesis), thus allowing an easy retrieval of encoded information by a low cortical activity, as revealed by alpha ERD (in line with “neural efficiency” hypothesis). To reconcile this contrasting evidence, EEG data were collected during a working memory task in which we focused on encoding and retrieval phases. We evaluated the relationships among the theta ERS, the alpha ERD, and the subjects’ IQ in both phases. Specifically, the encoding phase pertained to a match to sample task, whereas the retrieval phase included a delayed match to sample, with a possible requirement for mental spatial rotation in both phases. As a novelty, this design minimized the differences as graphical features and motor outputs of the two phases. Furthermore, it used the same male subjects for the encoding and retrieval tasks, thus reducing the inter-subjects variability of the EEG results and the effects of cyclic female sexual hormones on brain responses and cognitive processes.