Temporal Frequency of Whisker Movement. II. Laminar Organization of Cortical Representations

Abstract

Part of the information obtained by rodent whiskers is carried by the frequency of their movement. In the thalamus of anesthetized rats, the whisker frequency is represented by two different coding schemes: by amplitude and spike count (i.e., response amplitudes and spike counts decrease as a function of frequency) in the lemniscal thalamus and by latency and spike count (latencies increase and spike counts decrease as a function of frequency) in the paralemniscal thalamus (see accompanying paper). Here we investigated neuronal representations of the whisker frequency in the primary somatosensory ("barrel") cortex of the anesthetized rat, which receives its input from both the lemniscal and paralemniscal thalamic nuclei. Single and multi-units were recorded from layers 2/3, 4 (barrels only), 5a, and 5b during vibrissal stimulation. Typically, the input frequency was represented by amplitude and spike count in the barrels of layer 4 and in layer 5b (the "lemniscal layers") and by latency and spike count in layer 5a (the "paralemniscal layer"). Neurons of layer 2/3 displayed a mixture of the two coding schemes. When the pulse width of the stimulus was reduced from 50 to 20 ms, the latency coding in layers 5a and 2/3 was dramatically reduced, while the spike-count coding was not affected; in contrast, in layers 4 and 5b, the latencies remained constant, but the spike counts were reduced with 20-ms stimuli. The same effects were found in the paralemniscal and lemniscal thalamic nuclei, respectively (see accompanying paper). These results are consistent with the idea that thalamocortical loops of different pathways, although terminating within the same cortical columns, perform different computations in parallel. Furthermore, the mixture of coding schemes in layer 2/3 might reflect an integration of lemniscal and paralemniscal outputs.

Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex

“…The L5A pyramidal cells are excited by thalamic afferents from the POm (Chmielowska et al, 1989;Lu and Lin, 1993;Ahissar et al, 2000Ahissar et al, , 2001 and, in addition, by intracortical inputs from layer 4 described here as well as from layer 2/3 and layer 5A (Feldmeyer, unpublished observation). Thus, the excitation conveyed by lemniscal and paralemniscal thalamic projections, also termed "specific" and "unspecific," is merging in L5A, as shown schematically in Figure 7, A and B.…”

“…Thus, it is likely that the earliest input to L5A cells is provided by L4 spiny neurons, which is then followed by an asynchronous L2/3 input. The paralemniscal input to layer 5A is active even later, at least under conditions of anesthesia (Ahissar et al, 2000(Ahissar et al, , 2001. Whisker responses in septum-related neurons receiving direct paralemniscal input were found to have a clearly longer latency than those in L2/3 pyramidal cells receiving lemniscal input (23 vs 10 ms) (Brecht et al, 2003).…”

“…Functional evidence indicates that the temporal response characteristics are similar for POm thalamic neurons and L5A pyramidal cells. This has been taken to suggest that these neurons are a component of the more slowly responding paralemniscal system operating in parallel to the rapidly reacting lemniscal system (Kim and Ebner, 1999;Ahissar et al, 2000Ahissar et al, , 2001. A possible integration of the lemniscal and paralemniscal inputs may then occur at the level of layer 2/3 (Ahissar et al, 2001;Ahissar and Kleinfeld, 2003).…”

Stimulus frequency dependence of blood oxygenation level-dependent functional magnetic resonance imaging signals in the somatosensory cortex of rats

“…However, the BOLD signal peaked at an intermediate stimulus frequency during forepaw stimulation even in the gradient-echo EPI experiments at 7 T with a longer stimulus pulse width (i.e., 10 ms) (Van Camp et al, 2006). This stimulus frequency dependence may be explained on the basis of evidence suggesting that at high magnetic field strengths (>7 T), the contribution of large blood vessels decreases relative to the effect of small vessels Yacoub et al 2003); another explanation may be that neuronal responses vary according to the stimulus pulse width (Ahissar et al, 2001), which affects BOLD signals (Logothetis et al, 2001;Smith et al, 2002).…”

Developmental and comparative aspects of posterior medial thalamocortical innervation of the barrel cortex in mice and rats

“…This pathway—the so-called paralemniscal pathway—conveys signals related to vibrissal movement (Ahissar et al, 2000; Yu et al, 2006). Thus, in rats the two thalamic streams form largely non-overlapping, complementary patterns of terminations in and outside of layer IV, thereby establishing semi-independent circuits for tactile information processing (Koralek et al, 1988; Chmielowska et al, 1989; Lu and Lin, 1993; Kim and Ebner, 1999; Ahissar et al, 2001; Bureau et al, 2006). …”