Differential Roles of Frequency-following and Frequency-doubling Visual Responses Revealed by Evoked Neural Harmonics

Abstract

Frequency-following and frequency-doubling neurons are ubiquitous in both striate and extrastriate visual areas. However, responses from these two types of neural populations have not been effectively compared in humans because previous EEG studies have not successfully dissociated responses from these populations. We devised a light–dark flicker stimulus that unambiguously distinguished these responses as reflected in the first and second harmonics in the steady-state visual evoked potentials. These harmonics revealed the spatial and functional segregation of frequency-following (the first harmonic) and frequency-doubling (the second harmonic) neural populations. Spatially, the first and second harmonics in steady-state visual evoked potentials exhibited divergent posterior scalp topographies for a broad range of EEG frequencies. The scalp maximum was medial for the first harmonic and contralateral for the second harmonic, a divergence not attributable to absolute response frequency. Functionally, voluntary visual–spatial attention strongly modulated the second harmonic but had negligible effects on the simultaneously elicited first harmonic. These dissociations suggest an intriguing possibility that frequency-following and frequency-doubling neural populations may contribute complementary functions to resolve the conflicting demands of attentional enhancement and signal fidelity—the frequency-doubling population may mediate substantial top–down signal modulation for attentional selection, whereas the frequency-following population may simultaneously preserve relatively undistorted sensory qualities regardless of the observer’s cognitive state.

Audio-visual synchrony and feature-selective attention co-amplify early visual processing

“…This difference likely relates to findings that harmonics constitute genuine neural responses that code complementary rather than redundant stimulus representations (Pastor et al 2007;Jenkins et al 2011;Kim et al 2011). Further corroborating these findings, we found individual fundamental and harmonic SSR amplitudes to be uncorrelated.…”

“…Notably, spectra revealed strong harmonic responses at twice the pulse frequencies (6.28 and 7.24 Hz). We included these pulsedriven harmonics in further analyses because fundamental and harmonic responses have been repeatedly found to reflect different aspects of stimulus processing (Pastor et al 2007;Kim et al 2011;Porcu et al 2013). …”

The Selectivity of Task-Dependent Attention Varies with Surrounding Context

“…To take into account the difference in noise levels between the recordings from each of our observers (Vialatte et al, 2010), we computed the signal-to-noise ratio (SNR) by dividing peak amplitudes by the associated noise, which is defined for a given frequency f by the average amplitude of the two neighbor frequencies (i.e., f Ϫ ␦f and f ϩ ␦f where ␦f gives the frequency resolution of the Fourier analysis, which was 0.5 Hz in our studies). Our analysis focused on the second-harmonic components of the flicker frequencies (i.e., 2f ) because previous studies have found the second-harmonic response to be particularly robust in the SSVEP (Rager and Singer, 1998;Herrmann, 2001;Pei et al, 2002) and highly sensitive for attentional modulation (Pei et al, 2002;Kim et al, 2007Kim et al, ,2011Pastor et al, 2007;Saupe et al, 2009). Indeed, SNRs of the first-harmonic components were either very poor (SNR Ͻ Ͻ 1.5) or did not show any attentional modulations in this experiment.…”

The steady-state visual evoked potential reveals neural correlates of the items encoded into visual working memory

“…Secondly, it may be that the perceptual and cognitive processes underlying VWM encoding operate preferentially on contrast-rectified representations of the stimuli (at least in the context of the stimuli as presented in our task). Indeed, several recent studies have analyzed the second harmonic frequency when using the SSVEP technique concurrent with contrast-reversed stimuli (e.g., black-white pattern reversal (Garcia, Srinivasan, & Serences, 2013; Kim, Grabowecky, Paller, & Suzuki, 2011). Additionally, Kim and colleagues (2011) recently found evidence suggesting that visual-spatial attention modulates the second, but not first, harmonic frequency of the SSVEP signal.…”