Slow-Wave Activity in the S1HL Cortex Is Contributed by Different Layer-Specific Field Potential Sources during Development

Abstract

Spontaneous correlated activity in cortical columns is critical for postnatal circuit refinement. We used spatial discrimination techniques to explore the late maturation of synaptic pathways through the laminar distribution of the field potential (FP) generators underlying spontaneous and evoked activities of the S1HL cortex in juvenile (P14–P16) and adult anesthetized rats. Juveniles exhibit an intermittent FP pattern resembling Up/Down states in adults, but with much reduced power and different laminar distribution. Whereas FPs in active periods are dominated by a layer VI generator in juveniles, in adults a developing multipart generator takes over, displaying current sinks in middle layers (III–V). The blockade of excitatory transmission in upper and middle layers of adults recovered the juvenile-like FP profiles. In addition to the layer VI generator, a gamma-specific generator in supragranular layers was the same in both age groups. While searching for dynamical coupling among generators in juveniles we found significant cross-correlation in ∼one-half of the tested pairs, whereas excessive coherence hindered their efficient separation in adults. Also, potentials evoked by tactile and electrical stimuli showed different short-latency dipoles between the two age groups, and the juveniles lacked the characteristic long latency UP state currents in middle layers. In addition, the mean firing rate of neurons was lower in juveniles. Thus, cortical FPs originate from different intra-columnar segments as they become active postnatally. We suggest that although some cortical segments are active early postnatally, a functional sensory-motor control relies on a delayed maturation and network integration of synaptic connections in middle layers.SIGNIFICANCE STATEMENT Early postnatal activity in the rodent cortex is mostly endogenous, whereas it becomes driven by peripheral input at later stages. The precise schedule for the maturation of synaptic pathways is largely unknown. We explored this in the somatosensory hindlimb cortex at an age when animals begin to use their limbs by uncovering the laminar distribution of the field potential generators underlying the dominant delta waves in juveniles and adults. Our results suggest that field potentials are mostly generated by a pathway in deep layers, whereas other pathways mature later in middle layers and take over in adults. We suggest that a functional sensory-motor control relies on a delayed maturation and network integration of synaptic connections in middle layers.

Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks

“…Recordings were carried out while the animal freely explored a familiar open field (Figures 1, 2, 3, 4, 5, 6), a novel open field (Figure 6) or a T-maze (Figure 7). Using spatial discrimination techniques to separate LFP sources contributed by different synaptic pathways, based on independent component analysis (ICA, Figure 1—figure supplement 1 ; Benito et al, 2014 ; Fernández-Ruiz and Herreras, 2013 ; Herreras, 2016 ; Herreras et al, 2015 ; Lęski et al, 2010 ; Makarov et al, 2010 ; Makarova et al, 2011 ; Ortuño et al, 2019 ; Schomburg et al, 2014 ), we dissected three robust components in all subjects ( Figure 1 ; Materials and methods). The maximum voltages ( Figure 1b ) and dipoles in the current source density (CSD) depth profiles ( Figure 1c ) of the three components matched the stratified distribution of known terminal fields in the hippocampus and the currents resulting from stimulation of the corresponding pathways, as previously shown ( Benito et al, 2014 ; Fernández-Ruiz and Herreras, 2013 ; Lasztóczi and Klausberger, 2014 ; Schomburg et al, 2014 ).…”

Magnetoencephalography can reveal deep brain network activities linked to memory processes

“…However, they may not recover the correct time‐course of each area during ongoing field potentials (Fernández‐Ruiz & Herreras, 2013; Martín‐Vázquez et al, 2013) as, for instance, close generators with uncorrelated activities would cancel the resultant current. BSS methods have been proposed as a powerful methodology to extract the time course associated with different sources, either local or propagated, with promising results in the rat hippocampus and cortex (López‐Madrona et al, 2020; Makarov et al, 2010; Ortuño et al, 2019). Nevertheless, the interpretation of the different components is not straightforward and requires prior knowledge of the brain sources and the geometrical propagation of the fields in order to correctly infer the origin of the components (Herreras et al, 2015).…”

Functional Interactions between Entorhinal Cortical Pathways Modulate Theta Activity in the Hippocampus

“…Moreover, it has been proposed as a tool to disentangle deep brain activities hidden at the surface by superficial signals with higher amplitudes [ 37 ]. Although its use in intracranial recordings is reduced in comparison, its effectiveness has been well studied [ 31 , 38 ], and it has been used to dissociate local and remote cortical field potentials [ 39 , 40 ] and different current generators in the hippocampus [ 7 , 16 , 41 , 42 ].…”