Tightly coupled inhibitory and excitatory functional networks in the developing primary visual cortex

Abstract

Intracortical inhibition plays a critical role in shaping activity patterns in the mature cortex. However, little is known about the structure of inhibition in early development prior to the onset of sensory experience, a time when spontaneous activity exhibits long-range correlations predictive of mature functional networks. Here, using calcium imaging of GABAergic neurons in the ferret visual cortex, we show that spontaneous activity in inhibitory neurons is already highly organized into distributed modular networks before visual experience. Inhibitory neurons exhibit spatially modular activity with long-range correlations and precise local organization that is in quantitative agreement with excitatory networks. Furthermore, excitatory and inhibitory networks are strongly co-aligned at both millimeter and cellular scales. These results demonstrate a remarkable degree of organization in inhibitory networks early in the developing cortex, providing support for computational models of self-organizing networks and suggesting a mechanism for the emergence of distributed functional networks during development.

Synapse-type-specific competitive Hebbian learning forms functional recurrent networks

“…43,44 Recent experimental results have suggested that inhibitory neurons drive decorrelation of neural activities. 45,46 In line with these results, in our model, interconnected inhibitory neurons repel each other and their tuning curves decorrelate (Fig. 2D).…”

Development of visual response selectivity in cortical GABAergic interneurons

“…At eye opening, excitatory networks display modular patterns of activity for both spontaneous and evoked activity, and initial cellular orientation preferences are already established 4 , 6 , 7 . A recent study suggested that GABA-INs also display modular patterns of spontaneous activity before eye opening 21 . In contrast, we show that modular patterns are not evident for visually-evoked activity and orientation tuning is not well established for GABA-INs at eye opening.…”

The development of bi-directionally coupled self-organizing neurovascular networks captures orientation-selective neural and hemodynamic cortical responses

“…The lateral connectivity of cortical neurons is known [27] to have an ON center OFF surround neighborhood connectivity. But the only hint that the tuned response in vessels gives is that there is a possibility of competitive learning among them, most likely brought about by inhibitory lateral connections [16]. To verify this, we varied the lateral architecture of vessels in the NV-LIN in three possible ways, (i) No lateral connectivity, (ii) ON center OFF surround, and (iii) OFF center ON surround.…”

“…In computational neural models, orientation selectivity of neurons often arises from the competitive learning facilitated by the distant lateral inhibitory connections [27]. Latest experimental studies also support the existence of such long range inhibitory connections among cortical neurons facilitating the self-organizing ability of the cortex during the developmental stage [16]. Since the vascular network also exhibits tuned responses, it indicates the possibility of inhibitory lateral connections among the vessels, which enable competitive learning.…”

“…Computational studies have shown that a neural network is capable of generating tuned responses to input stimuli by means of competitive learning, which can be implemented in a neural network by lateral interactions among the neurons characterized by long range inhibitory signaling and local excitatory signaling, often described as an ON-Center, OFF-surround neighborhood interaction [11][12][13]. The existence of the lateral excitatory and inhibitory connections among cortical neurons was supported by experimental studies [14][15][16][17]. A recent study shows the relevance of tightly coupled excitatory and inhibitory networks in the developing visual cortex with self-organizing ability.…”