Visual areas exert feedforward and feedback influences through distinct frequency channels

Abstract

However, although these studies have revealed the anatomical paths and the neurophysiological consequences of influences in both directions, the neurophysiological mechanisms through which these influences are exerted remain largely elusive. Here we show that in the primate visual system, feedforward influences are carried by thetaband (~4 Hz) and gamma-band (~60-80 Hz) synchronization, and feedback influences by beta-band (~14-18 Hz) synchronization. These frequency-specific asymmetries in directed influences were revealed by simultaneous local field potential recordings from eight visual areas and an analysis of Granger-causal influences across all 28 pairs of areas. The asymmetries in directed influences correlated directly with asymmetries in anatomy and enabled us to build a visual cortical hierarchy from the influence asymmetries alone. Across different task periods, most areas stayed at their hierarchical position, whereas particularly frontal areas moved dynamically. Our results demonstrate that feedforward and feedback signalling use different frequency channels, which might subserve their differential communication requirements and lead to differential local consequences. The possibility to infer hierarchical relationships through functional data alone might make it possible to derive a cortical hierarchy in the living human brain.Many aspects of cognitive performance can only be explained through the concept of feedback influences. For example, reaction times are shortened when stimulus locations are pre-cued and attention can be pre-directed, an effect that cannot be explained if only constant feedforward input is considered 3 . Numerous neurophysiological studies have demonstrated the effects of feedback influences on neuronal activity 2 , yet the mechanisms through which feedback influences are exerted remain elusive. Anatomical studies have revealed that structural connections in the feedforward direction, i.e. from the primary sensory areas to higher order areas, are complemented by connections in the feedback direction 1,4 . In addition, it is well established that feedforward and feedback connections follow a characteristic pattern with regard to cortical layers: Feedforward connections target the granular layer 1 ; they originate preferentially in supragranular layers, and this preference is stronger for projections traversing more hierarchical levels, i.e. it is quantitatively related to the hierarchical distance 4 .Feedback connections avoid targeting the granular layer 1 ; they originate preferentially in the infragranular layers, and again, this preference is stronger for projections traversing more hierarchical levels and is thereby quantitatively related to hierarchical distance 4 . These asymmetries have been used to arrange the visual cortical areas into a hierarchy 1,4 , which has influenced many theories of cognition and brain function 5,6 .Recent studies have documented a neurophysiological asymmetry between cortical layers in visual cortex: While supragranular layers show local gam...

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

“…The feedforward signature of γ is in line with recent studies showing stronger Granger causality for γ from V1 to V2 and from V1 to V4 than in the opposite direction (18,49,65). It is also reminiscent of a study in cats, showing that γ-oscillations propagate from the LGN to V1 with an average delay of ∼2 ms (47).…”

Direction of information flow in large-scale resting-state networks is frequency-dependent

“…2) are, for example, consistent with animal recordings that have shown cortico-hippocampal propagation at low frequencies and cortico-cortical propagation at higher frequencies (49). Similarly, bottom-up and top-down influences through distinct fast-and slow-frequency channels have also been reported for the visual system (45,50). Although these observations from task-based invasive animal recordings suggest that similar mechanisms may play a role during noninvasive resting-state recordings in humans, more work is needed to further elucidate the functional role of resting-state information flow through distinct frequency channels.…”

“…At the same time, this model predicts that anterior-to-posterior alpha connectivity provides a gating mechanism for attention, because top-down modulation by alpha could inhibit irrelevant activity (43,44). This may seem to be in disagreement with our findings of a posterior-toanterior dominant pattern of information flow in the alpha band, although it is possible that the enhanced bottom-up signaling in the alpha band is in itself a consequence of enhanced top-down signaling in the theta band (45). Moreover, one should take into consideration that our recordings were resting state and not taskbased, and that neuronal signatures of different forms of attention (46) are assumed to be related but can have different spatiotemporal and frequency contents.…”

“…The opposite pattern was observed in the theta (4-8 Hz) band (PAx = −0.50, P < 0.001). The patterns in the gamma (30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48) and delta (0.5-4 Hz) bands were more dispersed [although still significant (P < 0.001); PAx = 0.26 and −0.29, respectively]. We describe the results for the alpha2 and theta band in more detail below, as the patterns for these bands (i) were most pronounced and (ii) resulted in high PAx values.…”

MEG-measured visually induced gamma-band oscillations in chronic schizophrenia: Evidence for impaired generation of rhythmic activity in ventral stream regions

“…More specifically, high frequency oscillations occur predominantly in granular layers 3 and 4, while alpha (8-12 Hz)/beta (13-30 Hz) oscillations occur predominantly in infra-granular layers 5 and 6 (Bastos et al, 2015;van Kerkoerle et al, 2014). In addition to stimulus parameters, the amplitude and frequency of high-frequency oscillations in visual cortices can also be influenced by central states, such as attention.…”