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NEUROSCIENCE
1
NEUROSCIENCE FOREFRONT REVIEW
G. López-Bendito / Neuroscience xxx (2018) xxx–xxx

3
2 Development of the Thalamocortical Interactions: Past, Present and Future
4 Guillermina López-Bendito
5 Instituto de Neurociencias de Alicante, Universidad Miguel Hernández-Consejo Superior de Investigaciones Cientı´ficas (UMH-CSIC), Sant
6 Joan d’Alacant, Spain
7

9
8 Abstract—For the past two decades, we have advanced in our understanding of the mechanisms implicated in the
formation of brain circuits. The connection between the cortex and thalamus has deserved much attention, as tha-
lamocortical connectivity is crucial for sensory processing and motor learning. Classical dye tracing studies in
wild-type and knockout mice initially helped to characterize the developmental progression of this connectivity
and revealed key transcription factors involved. With the recent advances in technical tools to specifically label
subsets of projecting neurons, knock-down genes individually and/or modify their activity, the field has gained
further understanding on the rules operating in thalamocortical circuit formation and plasticity. In this review, I
will summarize the most relevant discoveries that have been made in this field, from development to early plas-
ticity processes covering three major aspects: axon guidance, thalamic influence on sensory cortical specifica-
tion, and the role of spontaneous thalamic activity. I will emphasize how the implementation of new tools has
helped the field to progress and what I consider to be open questions and the perspective for the future. Ó
2018 IBRO. Published by Elsevier Ltd. All rights reserved.

Key words: thalamus, axon guidance, spontaneous activity, somatosensory system, cortical maps, calcium waves.

10 INTRODUCTION cortical areas. More recently, the application of novel 32


techniques in this field, such as the use of conditional 33
11 The thalamocortical system has been widely used as a mouse lines or in utero electroporation, has greatly 34
12 model to study basic axon guidance mechanisms, contributed to our understanding on the role of TCAs in 35
13 decipher the factors involved in the development of cortical development and sensory function (Fig. 1A). 36
14 cortical maps, understand how sensory systems Here, I will give an outline of the major discoveries 37
15 develop, and study the mechanisms involved in made in the thalamocortical system, and then review 38
16 anatomical and functional circuit plasticity following the technical advances that have rapidly helped discern 39
17 sensory loss. The reason for this great interest is due to the role of intrinsic and extrinsic (mainly thalamic) 40
18 the unique anatomical and functional specificities of the mechanisms involved in the development of sensory 41
19 thalamus. Anatomically, thalamocortical axons (TCAs) cortical areas. The main themes covered are (i) axon 42
20 comprise a large ipsilateral projection, which develops guidance and the handshake hypothesis, (ii) the 43
21 embryonically crossing various anatomical boundaries. influence of sensory thalamic inputs to cortical 44
22 Thalamocortical neurons can be classified into two specification, and (iii) the role of spontaneous thalamic 45
23 broad types, those that are specific and topographically neural activity. 46
24 organized, mainly projecting to layer 4 of primary
25 cortical areas, and those that are multi-specific, less
26 topographically structured and massively innervating
AXON GUIDANCE TO THE CORTEX 47
27 layer 1 of extensive cortical regions. The functional role
28 of TCAs is central to sensory processing and perception At the end of the last century the ability to trace axons in 48
29 as they carry information received from the periphery to fixed embryonic tissue offered by the carbocyanine dye 49
30 specialized cortical areas. During development, specific technique was pioneering. Using these anterograde and 50
31 sensory thalamic projections help define functional retrograde tracers to label axons and cells, several 51
authors described for the first time the timing and 52
trajectory of thalamocortical connectivity and associated 53
Abbreviations: A1, auditory area; dLGN, dorsolateral geniculate projections (McConnell et al., 1989; Blakemore and 54
nucleus; DTB, diencephalic-telencephalic boundary; MGE, medial Molnar, 1990; Catalano et al., 1991; De Carlos and 55
ganglionic eminence; PSPB, pallial subpallial boundary; S1,
somatosensory area; TCAs, thalamocortical axons; V1, visual cortex;
O’Leary, 1992; Ghosh and Shatz, 1992; Agmon et al., 56

VPM, ventromedial posterior. 1995; Molnár, 1998; Molnar and Cordery, 1999). Briefly, 57
E-mail address: g.lbendito@umh.es thalamic axons exit the thalamus, traverse the 58

https://doi.org/10.1016/j.neuroscience.2018.06.020
0306-4522/Ó 2018 IBRO. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: López-Bendito G. Development of the Thalamocortical Interactions: Past, Present and Future. Neuroscience (2018), https://doi.org/10.1016/j.neuroscience.2018.06.020
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Fig. 1. Developmental timeline in the thalamocortical research. (A) Timeline representing the major discoveries in the field of thalamocortical
development over the past 40 years. The major techniques used to achieve those findings are highlighted. (B) Schemas representing four key
findings in the field that were made in the last few years. (1) The mechanism that allows rostral and intermediate TCAs to topographically arrange
depends on interaction of guidance cues and receptors at the corridor cells. (2) The velocity of axonal growth in TCAs is controlled by activity-
dependent gene expression. (3) The specification of a cortical area directly depends on the subtype of thalamic input that receives, being the higher-
order mode the default signature. Moreover, this thalamic influence depends on neurotransmitter release from thalamic neurons. (4) Prenatal
thalamic neurons are able to generate calcium waves of spontaneous activity among sensory nuclei that influence cortical areas size and plasticity.

59 pre-thalamus avoiding the hypothalamic region to cross the MGE and arrive at the cortex through the action of 86
60 the diencephalic-telencephalic boundary (DTB) to reach guidance molecules of the Nrg1 family. The position of 87
61 the subpallium. They then cross different anatomical terri- these corridor cells at the mantle of the MGE is controlled 88
62 tories, interact with other developing axons, and cross the by the midline repellent Slit2 (Bielle et al., 2011a). It is 89
63 pallial-subpallial boundary to enter the neocortex at believed that fine control of the location of these corridor 90
64 around E15.5 in mice (reviewed in (Lopez-Bendito and cells during evolution contributed to the switch from an 91
65 Molnár, 2003; Molnar et al., 2012; Leyva-Dı́az and external TCA pathway to the internal path that is charac- 92
66 Lopez Bendito, 2013; Garel and Lopez-Bendito, 2014)). teristic in mammals (Bielle et al., 2011a). 93
67 A new wave of discoveries was initiated in the late 90s Other cells also provide guidance information to 94
68 following the first anatomical description of the TCA TCAs. Neurons located at the prethalamic, perireticular 95
69 pathway. Using full knock-out mice for genes expressed and internal capsule regions, with early projections to 96
70 at the origin, along the pathway or in the target the thalamus, also influence TCAs’ pathfinding at the 97
71 structure, several transcription factors such as Emx2, DTB and subpallial levels (Mitrofanis and Guillery, 1993; 98
72 Pax6, Tbr1, Gbx2, Nkx2.1 or Ebf1 (Bishop et al., 2000; Metin and Godement, 1996; Molnar et al., 1998a). In fact, 99
73 Mallamaci et al., 2000; López-Bendito et al., 2002) were in mutant mice with displaced internal capsule projecting 100
74 identified as being involved in thalamocortical pathfinding cells, TCAs do not cross the DTB (López-Bendito et al., 101
75 (Bishop et al., 2000; Mallamaci et al., 2000; López- 2002). Our understanding of the role of striatal cells in 102
76 Bendito et al., 2002). Moreover, axon guidance molecules the guidance of TCAs at the subpallium is gaining impor- 103
77 were also implicated. To cross the DTB, TCAs need a Slit- tance, as many of their projections are located in the vicin- 104
78 mediated repulsion from the hypothalamus (Braisted ity of TCAs. Modification of the position of these striatal 105
79 et al., 1999; Bagri et al., 2002; López-Bendito et al., cells or their elimination leads directly to consistent TCAs’ 106
80 2007). Once in the subpallium, TCAs are attracted toward pathfinding errors (Uemura et al., 2007). They may influ- 107
81 the corridor, a dynamic region at the mantle of the medial ence TCAs’ trajectory indirectly by modifying the position 108
82 ganglionic eminence (MGE) populated by GABAergic of corridor cells in a Frizzled-dependent manner (Morello 109
83 neurons originated from the lateral ganglionic eminence et al., 2015). 110
84 (LGE) (Lopez-Bendito et al., 2006). This cellular bridge The guidance of TCAs is also influenced by early 111
85 provides a permissive environment for TCAs to cross pioneer cortical cells located in the subplate, a deep 112

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113 transient cortical cell population that projects to the (Fig. 1A). Gradients of axon guidance molecules such 172
114 thalamus (McConnell et al., 1989). It was proposed more as Netrin-1, Slit1, or Ephrin-A5 are expressed in register 173
115 than fifteen years ago that correct formation of thalamo- in both structures and play a role in the fine topographical 174
116 cortical reciprocal connectivity relies on the early interac- positioning of TCAs (Dufour et al., 2003; Bonnin et al., 175
117 tion between subplate axons and TCAs, the so called 2007; Powell et al., 2008; Bielle et al., 2011b; Leyva- 176
118 ‘handshake hypothesis’ formulated by Molnar and Blake- Diaz et al., 2014). However, a specific chemoattractive 177
119 more (Molnar and Blakemore, 1995) (Fig. 1A). By per- response is achieved at the corridor. By combining 178
120 forming tracing studies the authors showed the intimate in vitro chemotaxis assays with the analysis of TCA 179
121 anatomical apposition of cortical axons and TCAs at the defects in specific mutant mice, it was determined that 180
122 pallial subpallial boundary (PSPB), suggesting that these the rostral positioning of TCAs is achieved by a modula- 181
123 axons help guide each other (Molnar et al., 1998a,b). tion of Netrin-1 responsiveness by Slit1 at the corridor 182
124 However, this hypothesis remained under debate for dec- (Bielle et al., 2011b) (Fig. 1B, panel 1). Rostral TCAs 183
125 ades as other studies have shown that these axons only specifically express a novel Robo1 co-receptor, FLRT3, 184
126 interdigitate in some parts of their trajectory or can even which is a member of the Fibronectine leucine-rich repeat 185
127 repel each other in vitro (Miller et al., 1993; Bicknese transmembrane proteins. By a series of in vitro biochem- 186
128 et al., 1994; Bagnard et al., 2001). ical assays, it was shown that in the presence of Slit1, 187
129 In subsequent years, the field entered into an era of both Robo1 and FLRT3 receptors are required to induce 188
130 analyzing mutant mice in which thalamocortical Netrin-1 attraction, via the upregulation of DCC receptor 189
131 connectivity was affected by the lack of specific at the plasma membrane (Leyva-Diaz et al., 2014). Thus, 190
132 transcription factors (Fig. 1A). These studies did not TCAs expressing FLRT3 can modulate Netrin-1 respon- 191
133 however clarify whether the handshake hypothesis was siveness in a context-dependent manner in developing 192
134 correct, since the overall results were contradictory. TCAs. 193
135 Some of the mutant mice, such as Gbx2 or Pax6, did It is more than likely that the specific expression of 194
136 show deficits in TCAs’ pathfinding while in others, either axon guidance receptors in the distinct TCA 195
137 the development of corticofugal axons was normal subpopulations is genetically determined by unique 196
138 (Mash-1) or both corticofugal axons and TCAs were transcription factors either alone or in combination. For 197
139 severely affected (Emx2 and Tbr1) (Stoykova et al., example, Lhx2, a transcription factor of the LIM 198
140 1996; Tuttle et al., 1999; Hevner et al., 2002; Jones homeodomain family is expressed by all early 199
141 et al., 2002; López-Bendito et al., 2002). Conditional postmitotic thalamic neurons but downregulated in a 200
142 mutagenesis has recently shed light on this issue and region-specific manner at a late postmitotic stage 201
143 supported the subpallial interaction between both axonal (Marcos-Mondejar et al., 2012). While only rostral and 202
144 tracts as a pre-requisite for their correct development. intermediate thalamic neurons switch off Lhx2, this tran- 203
145 When the maturation of cortical progenitors was abol- scription factor remains active only in thalamic neurons 204
146 ished in a cortex-dependent manner, without affecting from the auditory nucleus (Marcos-Mondejar et al., 205
147 the thalamus or any other subpallial structure, postmitotic 2012). When Lhx2 was ectopically upregulated in rostral 206
148 neurons were unable to generate corticofugal axons lead- or intermediate thalamic nuclei, TCAs from those territo- 207
149 ing to a scenario in which TCAs do not progress through ries fail to reach their corresponding cortical areas and 208
150 the PSPB and thus, do not reach the cortex (Chen et al., abnormally acquire an auditory fate targeting A1 209
151 2012). The opposite genetic experiment was carried out in (Marcos-Mondejar et al., 2012). These experiments sug- 210
152 parallel, using conditional ablation of the embryonic thala- gest that there must be a transcriptional code that deter- 211
153 mus and showed that TCAs are also required in vivo to mines the fate of thalamocortical neurons from the 212
154 guide corticothalamic axons into the corridor and thala- different sensory nuclei. In fact, the development of a 213
155 mus (Deck et al., 2013), thereby supporting the hand- genome-wide analysis has helped to test this possibility 214
156 shake hypothesis at least at a particular stage and through an unbiased approach. Using a genetic dual 215
157 region of the subpallium. labeling method in mice, Gezelius and colleagues purified 216
different sensory thalamic neurons and revealed their 217
transcriptome profiling. Genes such as Sp9, Hs6st2, 218

158 ACQUIRING TOPOGRAPHY Crabp2 or Cck, were found to be expressed at specific 219
sensory nuclei during embryonic development (Gezelius 220
159 One of the most important factors for the correct et al., 2016). Complementary studies using new genera- 221
160 functioning of the thalamocortical system is well tion sequencing revealed the transcriptional profile of 222
161 arranged topographical connectivity. TCAs from the the different sensory thalamic nuclei at early postnatal 223
162 distinct principal sensory-modality nuclei primarily target stages (Frangeul et al., 2016). 224
163 modality-matched cortical areas. The dorsolateral Several decades of intense debate have been spent 225
164 geniculate nucleus (dLGN) projects to the primary visual on understanding the mechanisms involved in cortical 226
165 cortex (V1), the ventromedial posterior (VPM) to the specification: the process that is involved in the 227
166 somatosensory area (S1) and the ventro-medial acquisition of specific anatomical and functional 228
167 geniculate nucleus (vMG) to the primary auditory area properties of the distinct cortical territories. The 229
168 (A1). This topography is acquired embryonically and at controversy was founded upon two opposing views. 230
169 two consecutive subpallial structures, the corridor and One postulated that the cortex was already specified at 231
170 the striatum (Garel et al., 2002; Leyva-Dı́az and Lopez the proliferative area by intrinsic factors (Protomap 232
171 Bendito, 2013; Garel and Lopez-Bendito, 2014)

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233 hypothesis, (Rakic, 1972)), and the second proposed that axonal targeting (Borodinsky et al., 2004; Hanson and 292
234 the different cortical regions are only specified by input Landmesser, 2004; Mizuno et al., 2007; Wang et al., 293
235 from the thalamic axons, with cortical neurons being born 2007; Demarque and Spitzer, 2010; Yamamoto and 294
236 equally (Protocortex hypothesis, (O’Leary, 1989)). It is Lopez-Bendito, 2012). Spontaneous activity in the form 295
237 well accepted that the positional identity of cortical areas of calcium activity in developing neurons and axon growth 296
238 occurs independently of the thalamus, as it generally pre- cones has gained much attention in the last years. The 297
239 cedes thalamocortical innervation (Grove and Fukuchi- development of novel techniques for imaging intracellular 298
240 Shimogori, 2003), however, as we will describe in more calcium ion concentration has helped to identify calcium 299
241 detail later in the text, TCA will influence the final anatom- as a second messenger inside the cell that mediates a 300
242 ical and functional organization of cortical territories at wide spectrum of cellular functions (Fig. 1A). Calcium 301
243 perinatal-early postnatal stages (Anton-Bolanos et al., spikes are produced at distinct frequencies by embryonic 302
244 2018). Intracortical mechanisms also guide TCAs to thalamic neurons and it is this parameter which encodes 303
245 specific cortical territories influencing their final topo- the transcriptional regulation of genes that modulate TCA 304
246 graphical disposition. The adaptation of the in utero elec- growth rate (Fig. 1B, panel 2). When TCAs traverse the 305
247 troporation technique as a gene delivery system in mouse subpallium their growth rate is increased and then decel- 306
248 embryo allowed gene manipulation in a time- and region- erates on reaching the cortex (Mire et al., 2012). This 307
249 specific manner (Saito and Nakatsuji, 2001; Tabata and change in axonal growth rate is controlled by a develop- 308
250 Nakajima, 2001; Shimogori and Ogawa, 2008). When mental decrease in the frequency of calcium spikes at 309
251 the regional identity of the subplate cells was shifted out the cell soma (Mire et al., 2012). The activity-dependent 310
252 of register with the respective cortical plate through in regulation of TCA growth occurs via the transcriptional 311
253 utero overexpression of Fgf8, TCAs tracked this shift by regulation genes Robo1 and Dcc. Robo1 acts as a brake 312
254 producing ectopic arbors in the ‘‘matching” subplate area while Dcc functions as an accelerator for growth (Mire 313
255 (Shimogori and Grove, 2005). These results strongly sug- et al., 2012; Castillo-Paterna et al., 2015). 314
256 gested the existence of positional information in the sub- Spontaneous neural activity is also influential in the 315
257 plate that guides TCAs to the correct cortical territory, process of axonal branch formation in the 316
258 and matched previous data describing the need for TCAs thalamocortical system. Pioneer work by Herrmann and 317
259 to interact with subplate cells in order to recognize cortical Shatz in the mid 90s showed that when the sodium 318
260 areas (Ghosh et al., 1990; Ghosh and Shatz, 1993; channel blocker tetrodotoxin (TTX) was infused into 319
261 Allendoerfer and Shatz, 1994; O’Leary et al., 1994; kitten V1 fewer branches of visual TCAs were formed in 320
262 Molnar et al., 1998b). Specific elimination of subplate cells V1(Herrmann and Shatz, 1995). Such activity- 321
263 in cat S1, showed that corresponding TCAs do not enter dependent branch formation was later corroborated first 322
264 in S1 or in any remaining sensory area with an intact sub- by the use of organotypic co-culture assays (Yamamoto 323
265 plate. Therefore, subplate cells are an essential cortical et al., 1989, 1992; Uesaka et al., 2007), and subsequently 324
266 check-point for the spatial guidance of TCAs. It is likely by specific genetic manipulation in vivo (Narboux-Neme 325
267 that this positional information depends on activity- et al., 2012; Li et al., 2013; Hayano et al., 2014; Suzuki 326
268 based competition among TCAs, as thalamic axons inter- et al., 2015). 327
269 act with subplate cells through functional synapses (Friauf
270 et al., 1990; Ghosh and Shatz, 1993; Allendoerfer and
271 Shatz, 1994; Kanold and Luhmann, 2010; INFLUENCING CORTICAL TERRITORIES, AREA 328
272 Constantinople and Bruno, 2013). TCAs have a remark- IDENTITY AND SIZE 329
273 able capacity to reorganize themselves as can be seen
274 in Semaphorin6A mutant mice. In this mouse, visual Although the patterning of cortical areas is grossly 330

275 TCAs are profoundly derailed during embryonic develop- achieved by intrinsic cortical mechanisms, 331

276 ment, provoking a topographical shift in the targeting of thalamocortical input has a critical role later in 332

277 somatosensory axons to V1 (Little et al., 2009). Postna- development when shaping and delineating cortical 333

278 tally, the misrouted dLGN axons reach the V1 through areas, both anatomically and functionally. As mentioned 334

279 alternative routes and re-establish a normal pattern of before, each cortical area is reciprocally connected with 335

280 thalamocortical connectivity (Little et al., 2009). a distinct subset of thalamic neurons which are located 336
in well-defined nuclei. Primary cortical areas have 337
typical cytoarchitectonical features, especially S1 and 338

281 CONTROLLING AXON GROWTH AND V1, and thus, have been extensively to understand the 339
role of thalamocortical input in shaping cortical 340
282 BRANCHING
differentiation. Within the sensory areas, there is a 341
283 As previously mentioned, TCAs are guided toward their topographical representation of the sensory periphery 342
284 correct targets by interaction with axon guidance on the cortical surface. This point-to-point representation 343
285 molecules and /or intermediate targets. Arriving on time on the cortical field is due to the fact that neighboring 344
286 to coincide with specific target cells is necessary in neurons respond to the activation of neighboring 345
287 order to achieve a functionally correct circuit. peripheral receptors. 346
288 Spontaneous activity, which is present in almost all One of the first demonstrations of peripheral input 347
289 brain structures at embryonic stages, has been shown impact on the development of sensory cortical areas 348
290 to influence early developmental processes such as came from seminal studies in the late 60s and early 349
291 neurotransmitter specification, axon pathfinding or 70s. Visual deprivation in newborn cats led to changes 350

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351 in the number of dLGN cells, the targeting of TCAs, and covery of the intrinsic capability of the thalamus to gener- 412
352 the functional cortical properties in V1 (Wiesel and ate thalamocortical spontaneous waves of activity 413
353 Hubel, 1965; Sherman et al., 1972, 1974). In the embryonically supports this view. Thalamic neurons of dif- 414
354 somatosensory system, when whisker follicles which con- ferent sensory modalities engage in prenatal communica- 415
355 vey input from the periphery to S1 were lesioned perina- tion by means of spontaneous calcium waves that 416
356 tally, the representation of the injured whiskers in the propagate to the cortex (Moreno-Juan et al., 2017). 417
357 barrel field was impaired or disappeared producing a con- Embryonic perturbation of these waves leads to changes 418
358 comitant increase in the size of barrels representing the in the size of cortical areas through the specific activity- 419
359 intact whiskers (Van der Loos and Woolsey, 1973; dependent regulation of genes in thalamocortical neurons 420
360 Weller and Johnson, 1975; Killackey et al., 1976). Impor- (Fig. 1B, panel 4). The enlargement of S1 that it is trig- 421
361 tantly, manipulation in later stages did not lead to map gered by the perturbation of the thalamic waves or elimi- 422
362 defects (Woolsey and Wann, 1976), providing strong evi- nation of the eyes occurs independently of sensory 423
363 dence that an intact periphery, before barrel pattern experience (Moreno-Juan et al., 2017) supporting again 424
364 becomes visible, is a basic condition for the development an early role for thalamocortical communication in the 425
365 of a normal map in S1. However, these studies could not development of cortical areas. 426
366 demonstrate whether the most relevant influencing devel- Although it is believed that spontaneous activity from 427
367 opment of cortical maps was the periphery itself or the the periphery drives the correlated patterns seen in 428
368 neural activity that flows through the system. Moreover, central stations (Colonnese and Khazipov, 2010; 429
369 the changes observed in cortical maps could be indirect Ackman et al., 2012; Siegel et al., 2012), the emergence 430
370 and due to alterations in subcortical territories such as of embryonic thalamic calcium waves is independent of 431
371 the thalamus. the peripheral input as thalamic waves persist in an 432
372 The development of conditional loss-of-function embryonic enucleated mouse model in which there is no 433
373 mouse models in which a specific gene is deleted in retinal input to the thalamus (Moreno-Juan et al., 2017). 434
374 cortical or thalamic neurons helped to determine the role However, it is possible that postnatally, activity from the 435
375 of thalamocortical input in the process of cortical map periphery might impose or coordinate the pattern of activ- 436
376 formation (Fig. 1A). Genetic manipulations of thalamic ity in developing sensory stations, including the thalamus. 437
377 structures, such as the decrease in size of the dLGN or Nonetheless, recent in vivo data describe the existence of 438
378 the ablation of the VPM nuclei, confirmed the a synchronized spontaneous activity in the barrel cortex in 439
379 importance of thalamic input as an extrinsic factor the form of patch-work patterns that occur independently 440
380 essential for the differentiation and establishment of of the periphery (Mizuno et al., 2018). 441
381 primary and secondary cortical territories in both visual
382 and somatosensory systems (Chou et al., 2013; Vue
383 et al., 2013; Pouchelon et al., 2014). In the absence of pri- CONCLUDING REMARKS & FUTURE 442
384 mary (first-order) TCAs, cortical areas will remain at the PERSPECTIVE 443
385 default differentiation stage, which is that of secondary
386 areas (Fig. 1B, panel 3). Thus, TCAs from the first-order I have focused on reviewing the mechanisms involved in 444

387 nuclei provide specific information for cortical area pat- the guidance, targeting and plasticity of thalamocortical 445

388 terning, implying the possibility of activity-dependent connectivity, with an emphasis on how development of 446

389 mechanisms. Indeed, perturbations in the neurotransmit- specific techniques has helped the field to understand 447

390 ter release of TCAs lead to the reduction or complete these processes. The rapid development of techniques 448

391 abolishment of the barrel-field in the somatosensory sys- such as in utero electroporation for the manipulation of 449

392 tem (Narboux-Neme et al., 2012; Li et al., 2013; Suzuki gene function in vivo, generation of specific Cre-lox 450

393 et al., 2015; Martini et al., 2018). mouse lines for controlling spatial and temporal 451

394 The above-mentioned results show that thalamic input targeting of genes and the incorporation of new 452

395 is critical for the development of the cortical sensory generation sequencing for transcriptomic analysis of 453

396 areas. However, the time at which TCAs are necessary specific neurons has been crucial. 454

397 to this process is less understood. In fact, the thalamic Some of the questions to be addressed in the near 455

398 influence over the formation of cortical sensory future might be the following. Would it be possible to 456

399 representations occurs much earlier than previously reprogram thalamocortical neurons from one sensory- 457

400 thought. By perturbing the embryonic topography of the modality subset to another, given that direct 458

401 TCAs at the basal ganglia, Lokmane and colleagues reprogramming of cortical postmitotic neurons has been 459

402 showed that the ordering of TCAs is required for the successfully achieved (Rouaux and Arlotta, 2013)? 460

403 transfer of the whisker representation to the barrel field Endogenous brain cells such as postnatal reactive astro- 461

404 (Lokmane et al., 2013). Somatosensory TCAs abnormally cytes have been reprogrammed into functional neurons 462

405 target V1 at embryonic stages recovering and rewiring in vitro (Heinrich et al., 2010, 2011) as well as in vivo 463

406 into S1 postnatally, but fail to form an anatomical and (Guo et al., 2014), at least in models of brain injury. 464

407 functional map in the barrel field (Lokmane et al., 2013; Unpublished data from our laboratory suggest that thala- 465

408 Lokmane and Garel, 2014). These results strongly sug- mic astrocytes can be reprogrammed into functional tha- 466

409 gest that the correct postnatal development of cortical lamic neurons in vitro (A. Herrero and G. López- 467

410 maps may depend on early prenatal events that involve Bendito, unpublished). If this were to be the case 468

411 a ‘‘memory” of the first thalamocortical interactions. Dis- in vivo, reprogrammed astrocytes could be used in a 469
future strategy to restore sensory circuits in sensory- 470

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471 deprived animal models later in life. Moreover, brain orga- Bicknese AR, Sheppard AM, O’Leary DD, Pearlman AL (1994) 530
472 noids offer an exceptional opportunity to study aspects of Thalamocortical axons extend along a chondroitin sulfate 531
proteoglycan-enriched pathway coincident with the neocortical 532
473 human brain development and disease (Arlotta, 2018).
subplate and distinct from the efferent path. J Neurosci 533
474 Sensory processing disorders have been widely associ- 14:3500–3510. 534
475 ated with neurodevelopmental disorders such as Autism Bielle F, Marcos-Mondejar P, Keita M, Mailhes C, Verney C, Nguyen 535
476 and Schizophrenia (Anderson et al., 2017; Linke et al., Ba-Charvet K, Tessier-Lavigne M, Lopez-Bendito G, Garel S 536
477 2018; Mikkelsen et al., 2018), but the mechanisms (2011a) Slit2 activity in the migration of guidepost neurons shapes 537
478 involved in their generation remain poorly understood. thalamic projections during development and evolution. Neuron 538

479 Future studies might involve the generation of brain orga- 69:1085–1098. 539
Bielle F, Marcos-Mondejar P, Leyva-Diaz E, Lokmane L, Mire E, 540
480 noids from patients with Autism Spectrum Disorder in Mailhes C, Keita M, Garcia N, Tessier-Lavigne M, Garel S, Lopez- 541
481 order to observe possible developmental errors in the for- Bendito G (2011b) Emergent growth cone responses to 542
482 mation of sensory circuits that may underlie the associ- combinations of Slit1 and Netrin 1 in thalamocortical axon 543
483 ated sensory processing disorders. In sum, now that we topography. Curr Biol 21:1748–1755. 544
484 understand the basic rules involved in the establishment Bishop KM, Goudreau G, O’Leary DD (2000) Regulation of area 545

485 of thalamocortical connectivity, we are in the privileged identity in the mammalian neocortex by Emx2 and Pax6. Science 546
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486 position of being able to engage with further challenges.
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487 ACKNOWLEDGMENTS Bonnin A, Torii M, Wang L, Rakic P, Levitt P (2007) Serotonin 551
488 The writing of this review has been motivated by the modulates the response of embryonic thalamocortical axons to 552
netrin-1. Nat Neurosci 10:588–597. 553
489 recent receipt of the IBRO Kemali International Prize for
Borodinsky L, Root C, Cronin J, Sann S, Gu X, Spitzer N (2004) 554
490 Research in the Field of Basic and Clinical Activity-dependent homeostatic specification of transmitter 555
491 Neuroscience. I thank the members of my laboratory for expression in embryonic neurons. Nature 429:523–530. 556
492 discussions and useful comments on the manuscript. I Braisted J, Tuttle R, O’leary D (1999) Thalamocortical axons are 557
493 thank Stuart Ingham for the English revision of the text. influenced by chemorepellent and chemoattractant activities 558
494 This work was supported by the Spanish MINECO localized to decision points along their path. Dev Biol 559

495 BFU2015-64432-R, the Spanish State Research Agency 208:430–440. 560


Castillo-Paterna M, Moreno-Juan V, Filipchuk A, Rodriguez- 561
496 through the ‘‘Severo Ochoa” Programme for Centres of Malmierca L, Susin R, Lopez Bendito G (2015) DCC functions 562
497 Excellence in R&D (SEV-2013-0317), the as an accelerator of thalamocortical axonal growth downstream of 563
498 PROMETEO/2017/149, and the European Commission spontaneous thalamic activity. EMBO Rep 16:851–862. 564
499 Grant ERC-2014-CoG-647012. G. L-B is an EMBO YIP Catalano SM, Robertson RT, Killackey HP (1991) Early ingrowth of 565
500 Investigator and a FENS-Kavli scholar. I apologize to thalamocortical afferents to the neocortex of the prenatal rat. P 566

501 the authors that could not be cited due to space Natl Acad Sci USA 88:2999–3003. 567
Chen Y, Magnani D, Theil T, Pratt T, Price DJ (2012) Evidence that 568
502 limitations.
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856
857 (Received 15 May 2018, Accepted 12 June 2018)
858 (Available online xxxx)

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